Article

Tempo and Pattern of Avian Brain Size Evolution

Authors:
  • Bruce Museum
  • Johns Hopkin University
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Abstract

Relative brain sizes in birds can rival those of primates, but large-scale patterns and drivers of avian brain evolution remain elusive. Here, we explore the evolution of the fundamental brain-body scaling relationship across the origin and evolution of birds. Using a comprehensive dataset sampling> 2,000 modern birds, fossil birds, and theropod dinosaurs, we infer patterns of brain-body co-variation in deep time. Our study confirms that no significant increase in relative brain size accompanied the trend toward miniaturization or evolution of flight during the theropod-bird transition. Critically, however, theropods and basal birds show weaker integration between brain size and body size, allowing for rapid changes in the brain-body relationship that set the stage for dramatic shifts in early crown birds. We infer that major shifts occurred rapidly in the aftermath of the Cretaceous-Paleogene mass extinction within Neoaves, in which multiple clades achieved higher relative brain sizes because of a reduction in body size. Parrots and corvids achieved the largest brains observed in birds via markedly different patterns. Parrots primarily reduced their body size, whereas corvids increased body and brain size simultaneously (with rates of brain size evolution outpacing rates of body size evolution). Collectively, these patterns suggest that an early adaptive radiation in brain size laid the foundation for subsequent selection and stabilization.

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... But the evolutionary history of how birds attained their large brain sizes and cognitive abilities, and what drove that evolution, has only been approached in piecemeal fashion in the past, hampered by a lack of both comprehensive phylogenies for the huge diversity of living birds and broad cross-species samples of brain sizes in living birds and their fossil relatives. This deficit has now been overcome in a landmark study [1] of avian brain evolution published in Current Biology by Dan Ksepka and a team of 40 of his fellow avian biologists, paleontologists and systematists. ...
... Ksepka and colleagues [1] compiled a monumental dataset of over 2000 avian brains. To brain-size data obtained from the literature, they added nearly 300 brain volumes generated from computed tomography scans of living and fossil birds, and their closest relatives among non-avian theropod dinosaurs. ...
... Raw values therefore have to be modified by estimating the inherited component in any species' individual values prior to statistical analysis. Using recently developed statistical methods that account for evolutionary relatedness in conjunction with a recent comprehensive phylogeny of birds [6], Ksepka and colleagues' [1] team examined their dataset for statistically significant shifts in either evolutionary rate or baseline grade changes. Amazingly -but perhaps not surprisingly -they find evidence for no less than eighteen such shifts across 150 million years of avian history, hinting at a complex picture of brain size evolution in response to a varying range of drivers from mass extinction to sensory and dietary specialization. ...
Article
A groundbreaking study of brain evolution across birds and dinosaurs reveals potential drivers of increased brain size including biogeography and ecology. The most dramatic change occurred in the Neoaves after the Cretaceous-Paleogene extinction rather than earlier in bird evolution.
... As observed in Figure 2, all the specimens studied here have larger brains than expected for their body mass except for G. ruficauda. Ksepka et al. (2020) found that, in relation to other Telluraves, ...
... Nevertheless, changes in encephalization are not only related to selection on brain size alone (Ksepka et al., 2020). Recent studies propose that high levels of encephalization might be a result of differential growth of individual brain regions, such as those observed in owls, which have expanded Wulst (Balanoff et al., 2016;Iwaniuk et al., 2004b;Smaers & Vanier, 2019). ...
... Another explanation may be the increase in cognitive complexity, as observed in parrots and corvids (Ksepka et al., 2020). This might be a convergent increase in not only relative brain volume but also neuron density, allowing additional brain pathways or the elaboration or increased acuity of existing pathways (Ksepka et al., 2020). ...
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We used three‐dimensional digital models to investigate the brain and endosseous labyrinth morphology of selected Neotropical Piciformes (Picidae, Ramphastidae, Galbulidae and Bucconidae). Remarkably, the brain morphology of Galbulidae clearly separates from species of other families. The eminentiae sagittales of Galbulidae and Bucconidae (insectivorous with high aerial maneuverability abilities) are smaller than those of the toucans (scansorial frugivores). Galbula showed the proportionally largest cerebellum, and Ramphastidae showed the least foliated one. Optic lobes ratio relative to the telencephalic hemispheres showed a strong phylogenetic signal. Three hypotheses were tested: (a) insectivorous taxa that need precise and fast movements to catch their prey, have well developed eminentiae sagittales compared to fruit eaters, (b) species that require high beak control would show larger cerebellum compared to other brain regions and higher number of visible folia and (c) there are marked differences between the brain shape of the four families studied here that bring valuable information of this interesting bird group. Hypotheses H1 and H2 are rejected, meanwhile H3 is accepted. We use 3D digital models of the brain cavity and inner ear of species of Picidae, Ramphastidae, Galbulidae and Bucconidae to better understand functional and ecological implications. We found marked differences among the brains of the four families, being G. ruficauda the most different one. Fruit eaters (Ramphastidae) had the biggest eminenta sagittales ratio. The cerebellum showed variable sizes and variable visible foliation among species. Only the optic lobe ratio has a phylogenetic signal.
... Previous studies have therefore mostly been limited to comparing residual variation along a stable slope [i.e., mean relative brain size or encephalization quotient (EQ), quantified through differences in the intercept of the evolu tionary allometry] (7,8). There is, however, evidence to suggest that changes in the slope (quantifying changes in brainbody covaria tion) may constitute an important additional source of comparative variation (9)(10)(11)(12). ...
... Such decoupling leads to increased variation available to selection, which, in turn, is expected to heighten flexibility in re sponse to selection (16). Recent work has shown that shifts in slope are paramount to explaining the brain's evolutionary diversification in birds (12), demonstrating that the selective response to increased variation is not restricted solely to changes in mean relative brain size but may also play out in terms of changes in brainbody covari ation. In mammals, shifts in brainbody covariation have been sug gested to occur in primates (9), carnivorans (17), marsupials, (18), and among mammalian orders (11). ...
... This tem poral clustering suggests that changes in the relative growth trajec tory of brain and body size were fundamental for mammalian diversification in the wake of the KPg mass extinction. This aligns with a pattern recently observed in birds (12), suggesting that eco logical radiation and subsequent niche expansion following the KPg mass extinction played a major role in shaping the trajectories by which both birds and mammals became the largestbrained ver tebrate classes. ...
Article
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Relative brain size has long been considered a reflection of cognitive capacities and has played a fundamental role in developing core theories in the life sciences. Yet, the notion that relative brain size validly represents selection on brain size relies on the untested assumptions that brain-body allometry is restrained to a stable scaling relationship across species and that any deviation from this slope is due to selection on brain size. Using the largest fossil and extant dataset yet assembled, we find that shifts in allometric slope underpin major transitions in mam-malian evolution and are often primarily characterized by marked changes in body size. Our results reveal that the largest-brained mammals achieved large relative brain sizes by highly divergent paths. These findings prompt a reevaluation of the traditional paradigm of relative brain size and open new opportunities to improve our understanding of the genetic and developmental mechanisms that influence brain size.
... As in extant mammals, the brain occupies nearly the entire cranial cavity in crown birds, and thus, these endocasts are used as accurate proxies for brain size and shape in these groups (Jerison, 1973;Haight and Nelson, 1987;De Miguel and Henneberg, 1998;Iwaniuk and Nelson, 2002;Watanabe et al., 2019;Early et al., 2020). Volumetric analyses of endocasts from avialan and non-avialan dinosaurs show that crown birds exhibit a derived allometric trend in brain-to-body size although some closely related non-avialan dinosaurs (e.g., oviraptorosaurs, troodontids) overlap in allometric trends with neornithine groups (Balanoff et al., 2013;Ksepka et al., 2020). Volumetric data of endocasts also indicate that each brain region evolved under different modes across avian and non-avian coelurosaurs, implying mosaic brain evolution (Balanoff et al., 2016b). ...
... The following figure supplement is available for Figure 2-figure supplement 1. PC morphospaces with full specimen labels. Figure 2 continued on next page 2014; Ksepka et al., 2020). Although size data from endocasts show partial overlap of crown birds and non-avialan coelurosaurs (Balanoff et al., 2013;Ksepka et al., 2020), high-density shape data discriminate these groups more clearly along PC1 axis, where lower PC1 scores in the morphospace (Figure 2a) are associated with expanded cerebrum, ventrally located optic lobe, more compact hindbrain, and greater dorsoventral flexion. ...
... Figure 2 continued on next page 2014; Ksepka et al., 2020). Although size data from endocasts show partial overlap of crown birds and non-avialan coelurosaurs (Balanoff et al., 2013;Ksepka et al., 2020), high-density shape data discriminate these groups more clearly along PC1 axis, where lower PC1 scores in the morphospace (Figure 2a) are associated with expanded cerebrum, ventrally located optic lobe, more compact hindbrain, and greater dorsoventral flexion. Lower PC2 scores correlate with wider cerebrum, dorsoventrally longer optic lobe, anteroposteriorly shorter cerebellum, and more dorsoventrally flexed medulla. ...
Article
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How do large and unique brains evolve? Historically, comparative neuroanatomical studies have attributed the evolutionary genesis of highly encephalized brains to deviations along, as well as from, conserved scaling relationships among brain regions. However, the relative contributions of these concerted (integrated) and mosaic (modular) processes as drivers of brain evolution remain unclear, especially in non-mammalian groups. While proportional brain sizes have been the predominant metric used to characterize brain morphology to date, we perform a high-density geometric morphometric analysis on the encephalized brains of crown birds (Neornithes or Aves) compared to their stem taxa—the non-avialan coelurosaurian dinosaurs and Archaeopteryx . When analyzed together with developmental neuroanatomical data of model archosaurs ( Gallus , Alligator ), crown birds exhibit a distinct allometric relationship that dictates their brain evolution and development. Furthermore, analyses by neuroanatomical regions reveal that the acquisition of this derived shape-to-size scaling relationship occurred in a mosaic pattern, where the avian-grade optic lobe and cerebellum evolved first among non-avialan dinosaurs, followed by major changes to the evolutionary and developmental dynamics of cerebrum shape after the origin of Avialae. Notably, the brain of crown birds is a more integrated structure than non-avialan archosaurs, implying that diversification of brain morphologies within Neornithes proceeded in a more coordinated manner, perhaps due to spatial constraints and abbreviated growth period. Collectively, these patterns demonstrate a plurality in evolutionary processes that generate encephalized brains in archosaurs and across vertebrates.
... For the interspecific comparison of avian brain size, published datasets of whole-brain size (volume or mass) and body mass, compiled by Sayol et al. (2018), Ksepka et al. (2020), and Fristoe et al. (2017), were used. When the same species was found in more than one dataset, the value was taken from one selected dataset. ...
... When the same species was found in more than one dataset, the value was taken from one selected dataset. The order of the priority was Sayol et al. (2018), Ksepka et al. (2020), and Fristoe et al. (2017). As the three studies collected some data from the same original papers, which were already averaged for each species, I did not calculate mean values from the two or three datasets. ...
... The classification of migratory or resident bird species followed that of Sayol et al. (2018) and Fristoe et al. (2017), which was based on distribution maps of each species obtained from BirdLife International (http://www.birdlife.org). For species with data from Ksepka et al. (2020), I performed resident or migrant classifications by referring to BirdLife International. ...
Article
Elucidating determinants of interspecies variation in brain size has been a long-standing challenge in cognitive and evolutionary ecology. As the brain is an energetically expensive organ, energetic tradeoffs among organs are considered to play a key role in brain size evolution. This study examined the tradeoff between the brain and locomotion in birds by testing the relationship between brain size, flight modes with different energetic costs (flapping and soaring), and migratory behavior, using published data on the whole-brain mass of 2,242 species. According to comparative analyses considering phylogeny and body mass, soarers, who can gain kinetic energy from wind shear or thermals and consequently save flight costs, have larger brains than flappers among migratory birds. Meanwhile, the brain size difference was not consistent in residents, and the size variation appeared much larger than that in migrants. In addition, the brain size of migratory birds was smaller than that of resident birds among flappers, whereas this property was not significant in soarers. Although further research is needed to draw a definitive conclusion, these findings provide further support for the energetic tradeoff of the brain with flight and migratory movements in birds and advance the idea that a locomotion mode with lower energetic cost could be a driver of encephalization during the evolution of the brain. This article is protected by copyright. All rights reserved
... Among extant birds, eye size has been proposed to be correlated with and may constrain deflection of the optic lobes and cerebrum, relative cerebrum size, and relative brain size (29,30). Despite the crown clade being marked by a derived brain shape, previous studies fail to recover shifts at the divergence of Aves in evolutionary rates of relative volume of either the total brain or individual regions (2,31). However, these studies necessarily exclude data from stem birds due to a dearth of samples, obscuring any evolutionary shifts that might have occurred along the >70-Ma branch separating the divergences of Avialae and Aves. ...
... If these stem birds are included, we recover an ancestral body mass of 2.4 kg (eagle-sized). Our results demonstrate the disproportionate effect that mostly large-bodied palaeognaths and non-avialan dinosaurs had on states recovered by previous studies at the crown node in the absence of data from stem birds (2,31). Total exclusion of any outgroup data results in an opposite phenomenon, with what are likely artificially low underestimates of ancestral avian body mass. ...
... The recovered shift in relative brain size from the divergence of Avialae to the divergence of extant birds is increasingly marked based on sampling strategy (Fig. 6B). Thus, it is perhaps expected that recent investigations have failed to detect a significant shift in evolutionary rates of either total or regional brain volume at or near the divergence of extant birds in the absence of data from the avian stem (2,31). Despite our increased body mass sampling along the avian stem, neuroanatomical data from these taxa remain lacking, suggesting that our estimates of ancestral avian brain size are likely still influenced by taxonomic bias. ...
Article
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Birds today are the most diverse clade of terrestrial vertebrates, and understanding why extant birds (Aves) alone among dinosaurs survived the Cretaceous-Paleogene mass extinction is crucial to reconstructing the history of life. Hypotheses proposed to explain this pattern demand identification of traits unique to Aves. However, this identification is complicated by a lack of data from non-avian birds. Here, we interrogate survivorship hypotheses using data from a new, nearly complete skull of Late Cretaceous (~70 million years) bird Ichthyornis and reassess shifts in bird body size across the Cretaceous-Paleogene boundary. Ichthyornis exhibited a wulst and segmented palate, previously proposed to have arisen within extant birds. The origin of Aves is marked by larger, reshaped brains indicating selection for relatively large telencephala and eyes but not by uniquely small body size. Sensory system differences, potentially linked to these shifts, may help explain avian survivorship relative to other dinosaurs.
... Note the robust and strongly curved unguals, short tail, and narial slit F I G U R E 3 Systematic position of wing-propelled diving birds (bolded) and their near outgroups in Aves. The tree is simplified from Ksepka et al. (2020) with the position of Cinclidae modified based on Oliveros et al. (2019) and the position of Plotopteridae based on Mayr et al. (2021) than WPD, including wading, probing, leaf turning, and rare aerial flycatching (del Hoyo et al., 2005). While there are a very limited number of additional examples of WPD among other clades of birds (e.g., some species of shearwaters; del Hoyo et al., 1992), only the five clades listed above are composed entirely of species that habitually use this locomotor behavior. ...
... Raw measurement data and analysis scripts have been made available online (see Supporting Information Materials and https://www.morphosource.org/projects/000377999). The following equations were used to analyze discrete data: Endocast reconstruction-The endocranial neuroanatomy of birds is highly variable and has been demonstrated to reflect not only phylogeny, but ecology and aspects of cognition (Georgi & Sipla, 2008;Iwaniuk & Hurd, 2005;Ksepka et al., 2020;Smith & Clarke, 2012;Witmer et al., 2008). The internal cavities of the braincase of American Dipper C. mexicanus (USNM 630605), Hermit Thrush C. guttatus (USNM 634096), and Samoan Starling A. atrifusca (Sturnidae; USNM 498061) were digitally highlighted and modeled in 3D using the segmentation tools in Avizo (Thermo Fisher Scientific; http://www. ...
... It is absolutely true that there could be differences in the underlying neural wiring that would be undetected in our analyses of endocasts, but certainly nothing can be discerned grossly, suggesting subtle neural changes imparting the marked behavioral shifts. Although there are slight differences in the endocranial anatomy and relative brain volume of volant alcids and stem-penguins relative to their non-WPD sister taxa, the most profound anatomical changes in those groups occur in flightless pan-alcids and more-derived extant penguin lineages (Ksepka et al., 2020;Proffitt et al., 2016;Smith & Clarke, 2012). The relative recency of the divergence of dippers from non-WPD passerines coupled with their retention of aerial flight may be partly responsible for the lack of neuroanatomical specialization in the clade. ...
Article
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Of the more than 6,000 members of the most speciose avian clade, Passeriformes (perching birds), only the five species of dippers (Cinclidae, Cinclus) use their wings to swim underwater. Among nonpasserine wing‐propelled divers (alcids, diving petrels, penguins, and plotopterids), convergent evolution of morphological characteristics related to this highly derived method of locomotion have been well‐documented, suggesting that the demands of this behavior exert strong selective pressure. However, despite their unique anatomical attributes, dippers have been the focus of comparatively few studies and potential convergence between dippers and nonpasseriform wing‐propelled divers has not been previously examined. In this study, a suite of characteristics that are shared among many wing‐propelled diving birds were identified and the distribution of those characteristics across representatives of all clades of extant and extinct wing‐propelled divers were evaluated to assess convergence. Putatively convergent characteristics were drawn from a relatively wide range of sources including osteology, myology, endocranial anatomy, integument, and ethology. Comparisons reveal that whereas nonpasseriform wing‐propelled divers do in fact share some anatomical characteristics putatively associated with the biomechanics of underwater “flight”, dippers have evolved this highly derived method of locomotion without converging on the majority of concomitant changes observed in other taxa. Changes in the flight musculature and feathers, reduction of the keratin bounded external nares and an increase in subcutaneous fat are shared with other wing‐propelled diving birds, but endocranial anatomy shows no significant shifts and osteological modifications are limited. Muscular and integumentary novelties may precede skeletal and neuroendocranial morphology in the acquisition of this novel locomotory mode, with implications for understanding potential biases in the fossil record of other such transitions. Thus, dippers represent an example of a highly derived and complex behavioral convergence that is not fully associated with the anatomical changes observed in other wing‐propelled divers, perhaps owing to the relative recency of their divergence from nondiving passeriforms.
... Corvids and parrots are regarded as the most innovative birds, a conclusion that is backed by ample experimental evidence 46,47,49,50 . These taxa also share both the highest inferred rates of brainbody size evolution among Neoaves and the steepest allometric slopes among all birds 51 . This contrasts with less innovative taxa Relationship between neuron numbers and innovation propensity for the entire brain and the pallium, cerebellum and brainstem, as predicted by models. ...
... like early-diverging birds (Palaeognathae, basal Neognathae), Anseriformes (waterfowl) and predatory core landbirds (hawks and eagles, falcons and owls), whose allometric exponents have diverged little from the ancestral avian grade and hence represent low-slope grades. To assess whether the proliferation of neurons in the pallium can explain deviations from the 'ancestral' allometric scaling relationship, we estimated the allometric exponents of the neuron numbers for clades with the highest slope and low-slope grades (sensu ref. 51 ); we then compared these with the allometric exponents for the cerebellum and brainstem. We find that while the allometric exponents for the cerebellum and brainstem were similar between the two slope-grade groups, clades that share a high slope tended to accumulate disproportionately more neurons in the pallium as they become larger ( Fig. 3 and Supplementary Figs. ...
... Although the number of neurons in the cerebellum scaled primarily with absolute brain size, the effect of total neuron numbers on relative brain size persisted because, in birds, larger brains contain increasing proportions of neurons in the pallium and decreasing proportions in the cerebellum and other brain regions 24 . Third, we provide an adaptive explanation for some of the patterns of brainbody covariation in deep time detected by ref. 51 : clades that have a higher brain-body slope than others tend to be the ones that are most innovative. A higher brain-body slope means that as body size gets bigger, the brain increases disproportionately more in size than it does in non-innovative clades; this increase in both absolute and relative brain size is, according to our analyses, mostly due to an increase in pallial neurons. ...
Article
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A longstanding issue in biology is whether the intelligence of animals can be predicted by absolute or relative brain size. However, progress has been hampered by an insufficient understanding of how neuron numbers shape internal brain organization and cognitive performance. On the basis of estimations of neuron numbers for 111 bird species, we show here that the number of neurons in the pallial telencephalon is positively associated with a major expression of intelligence: innovation propensity. The number of pallial neurons, in turn, is greater in brains that are larger in both absolute and relative terms and positively covaries with longer post-hatching development periods. Thus, our analyses show that neuron numbers link cognitive performance to both absolute and relative brain size through developmental adjustments. These findings help unify neuro-anatomical measures at multiple levels, reconciling contradictory views over the biological significance of brain expansion. The results also highlight the value of a life history perspective to advance our understanding of the evolutionary bases of the connections between brain and cognition. Using estimation data on neuron numbers in 111 bird species across 24 families, the authors show that number of neurons is positively associated with innovation propensity and encephalization.
... Brain-body allometry across species, which is referred to as evolutionary allometry, is an emergent property of the slope and the intercept of ontogenetic and static allometry and the covariance of these parameters with body size [Pélabon et al., 2013;Voje et al., 2014]. The universal and close fit of brain-body allometry to observations within and among species has triggered rigorous attempts to understand the causes of brain-body allometry and its consequences for brain size evolution [Dubois, 1897;Lapicque, 1907;Jerison, 1973;Gould, 1975;Martin, 1981;Striedter, 2005;Boddy et al., 2012;Montgomery et al., 2016;Tsuboi et al., 2018b;Mitov et al., 2019;Ksepka et al., 2020;Smaers et al., 2021]. ...
... Additionally, I demonstrated that the unique encephalization in this order results from evolutionary change in the slope of evolutionary brain-body allometry. I showed that the slope is virtually isometric (1.03 ± 0.09 SE), making it the steepest brain-body evolutionary allometry reported to date [Tsuboi et al., 2018b;Ksepka et al., 2020] along with hominins that appear to exhibit a similarly steep evolutionary allometry [1.10 ± 0.16; Smaers et al., 2021]. Furthermore, the dramatic steepening of the evolutionary allometric slope was a combined result of evolution in the slopes and intercepts of static allometry. ...
Article
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Brain-body static allometry, which is the relationship between brain size and body size within species, is thought to reflect developmental and genetic constraints. Existing evidence suggests that the evolution of large brain size without accompanying changes in body size (that is, encephalization) may occur when this constraint is relaxed. Teleost fish species are generally characterized by having close-fitting brain-body static allometries, leading to strong allometric constraints and small relative brain sizes. However, one order of teleost, Osteoglossiformes, underwent extreme encephalization, and its mechanistic bases are unknown. Here, I used a dataset and phylogeny encompassing 859 teleost species to demonstrate that the encephalization of Osteoglossiformes occurred through an increase in the slope of evolutionary (among-species) brain-body allometry. The slope is virtually isometric (1.03 ± 0.09 SE), making it one of the steepest evolutionary brain-body allometric slopes reported to date, and it deviates significantly from the evolutionary brain-body allometric slopes of other clades of teleost. Examination of the relationship between static allometric parameters (intercepts and slopes) and evolutionary allometry revealed that the dramatic steepening of the evolutionary allometric slope in Osteoglossiformes was a combined result of evolution in the slopes and intercepts of static allometry. These results suggest that the evolution of static allometry, which likely has been driven by evolutionary changes in the rate and timing of brain development, has facilitated the unique encephalization of Osteoglossiformes.
... intelligence j cognition j evolution j brain size j number of neurons The evolution of cognitive capacity or "intelligence" and its underlying neural substrate has been of long-standing interest to biologists. Great strides have been made in understanding the evolution of brain size in vertebrates, with studies analyzing data on thousands of species (1)(2)(3). Since larger animals have larger brains but are not necessarily smarter, most studies of cognitive evolution use relative brain size (corrected for body size), which is thought to reflect extra neurons beyond those needed for controlling the body (4). We now have a good idea where major changes in brain-body scaling happened within birds (2) and mammals (3), and it is also clear that both mammals and birds have relatively larger brains than nonavian sauropsids (hereafter referred to as reptiles), although this has been rarely formally quantified because data on reptilian brain sizes are scarce (5). ...
... For phylogenetic analyses, we adopted a phylogeny constructed from previously published species-level trees. We used recent published specieslevel time-calibrated phylogenies for squamates (71), birds (2), and mammals (72). For turtles and crocodiles, we used the Timetree of Life (73). ...
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Significance The evolution of brain processing capacity has traditionally been inferred from data on brain size. However, similarly sized brains of distantly related species can differ in the number and distribution of neurons, their basic computational units. Therefore, a finer-grained approach is needed to reveal the evolutionary paths to increased cognitive capacity. Using a new, comprehensive dataset, we analyzed brain cellular composition across amniotes. Compared to reptiles, mammals and birds have dramatically increased neuron numbers in the telencephalon and cerebellum, which are brain parts associated with higher cognition. Astoundingly, a phylogenetic analysis suggests that as few as four major changes in neuron–brain scaling in over 300 million years of evolution pave the way to intelligence in endothermic land vertebrates.
... In other animals, it is the adaptations of the central brains and existing CNS design that are more likely to retain a phylogenetically flavored relationship. 3,7,77 ...
... Complex flexible behaviors related to the vertical lobe Environmental and social complexity often plays a key role in the emergence of flexible adaptive behavior, leading to the evolution of advanced cognition and associating changes of brain regions. 4,56,77,[101][102][103] Unlike some social cuttlefish and squid that possess the lissencephalic VL, 13,57,104 octopodiforms have developed a variety of multi-gyri VLs, including an ancestral form of VL in V. infernalis; the 3-gyrus VL in mesopelagic octopus, Japetella diaphana; 8,71 5-gyrus VLs in coastal octopuses; 9,11,15,16,18 and the 7-gyrus species described here. This emergence of complexity provides another case to support the ideas of anatomical and functional convergence with parts of the vertebrate nervous system. ...
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Octopods are masters of camouflage and solve complex tasks, and their cognitive ability is said to approach that of some small mammals. Despite intense interest and some research progress, much of our knowledge of octopus neuroanatomy and its links to behavior and ecology comes from one coastal species, the European common octopus, Octopus vulgaris. Octopod species are found in habitats including complex coral reefs and the relatively featureless mid-water. There they encounter different selection pressures, may be nocturnal or diurnal, and are mostly solitary or partially social. How these different ecologies and behavioral differences influence the octopus central nervous system (CNS) remains largely unknown. Here we present a phylogenetically informed comparison between diurnal and nocturnal coastal and a deep-sea species using brain imaging techniques. This study shows that characteristic neuroanatomical changes are linked to their habits and habitats. Enlargement and division of the optic lobe as well as structural foldings and complexity in the underlying CNS are linked to behavioral adaptation (diurnal versus nocturnal; social versus solitary) and ecological niche (reef versus deep sea), but phylogeny may play a part also. The difference between solitary and social life is mirrored within the brain including the formation of multiple compartments (gyri) in the vertical lobe, which is likened to the vertebrate cortex. These findings continue the case for convergence between cephalopod and vertebrate brain structure and function. Notably, within the current push toward comparisons of cognitive abilities, often with unashamed anthropomorphism at their root, these findings provide a firm grounding from which to work.
... Allofeeding with transfer of nectar would strengthen the pair bond and I suggest that the same applies to water transfer between the couple. From nectar allofeeding to water allodrinking is a simple behavioral step for innovative and ingenious birds such as parrots (Collar 1997;Kaplan 2017;Ksepka et al. 2020). ...
Article
Food transfer (allofeeding) is part of courtship and bonding behaviors of several bird species in varied families worldwide. Bonding behavior among parrots and other birds includes mutual preening and food transfer. Herein, I report on water transfer (allodrinking) in a couple of Rainbow Lorikeets Trichoglossus moluccanus in a mangrove at urban Sydney, Australia. The couple drank water accumulated in a mangrove branch hole, after which the male preened the female’s nape. Then, the couple interlocked their bills crosswise and bobbed their heads slightly. The birds disconnected briefly, the female with a liquid layer over the tongue including the brush tip. The couple resumed bill interlocking, a large drop visible under the male’s tongue. As the crosswise bill movements proceeded, the male showed a drop within the bill and the female has a liquid layer over the bill edge. Only liquid transfer was noticed, no food particles. Rainbow Lorikeets feed mostly on nectar and pollen and mate for life, and I expect that lorikeets allofeed with nectar transfer while bonding. I suggest that the same applies to water transfer between the couple, and hypothesize on the situation suitable for the derivation of water sharing from courtship feeding.
... Extant corvid diversity includes more than 120 species with a global geographic distribution excluding only Antarctica, the southernmost portion of South America and a few isolated oceanic islands (del Hoyo et al., 2009;Winkler et al., 2020). Much of corvid evolutionary success and ecological plasticity has been attributed to their large brains and associated cognitive abilities and high degrees of sociality, with crows and ravens widely considered to be the most intelligent of all living birds, and capable of a variety of cognitively advanced behaviors (e.g., facial recognition, tool construction and use) that rival those of hominins (Melhorn et al., 2010;Ksepka et al., 2020). ...
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The nearly complete skull of a raven (Aves, Corvidae) is reported from middle Pleistocene sediments (∼450–580 ka) of Jinyuan Cave near the city of Dalian on the Liaodong Peninsula of Liaoning Province, China. The new fossil closely resembles that of the Common Raven (Corvus corax), a species with a Holarctic extant distribution. It is one of the relatively few fossil corvids known from China, and the first clear record of the Common Raven lineage in China. While the occurrence of this fossil raven is outside of the species current geographic distribution in China, the inferred paleohabitat for the cave setting as a dry and cold, shrub grassland is consistent with the preferred habitat of the living species. This raven likely was an omnivorous scavenger in the ecosystem surrounding the cave. The size of the skull places this individual in the larger end of the size range of extant ravens and is larger than most published European fossils. The combination of a relatively large interorbital fenestra and smaller suprameatic process in the fossil is similar to Asian specimens, potentially indicating phylogenetic relatedness. However, our study demonstrates that cranial osteological variation among extant Common Raven populations is little understood, particularly in a phylogenetic context.
... The transition from terrestrial theropod dinosaurs into volant modern birds (Neornithes) presents one of the most well-documented major transitions in evolutionary history [1][2][3][4][5][6]. The ability to locomote using powered flight, in which the wings generate lift and propulsive force, is a major innovation that expanded the ecological opportunities of early birds and contributed to their extant diversity [7,8]. ...
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Background: The origin of powered avian flight was a locomotor innovation that expanded the ecological potential of maniraptoran dinosaurs, leading to remarkable variation in modern birds (Neornithes). The avian sternum is the anchor for the major flight muscles and, despite varying widely in morphology, has not been extensively studied from evolutionary or functional perspectives. We quantify sternal variation across a broad phylogenetic scope of birds using 3D geometric morphometrics methods. Using this comprehensive dataset, we apply phylogenetically informed regression approaches to test hypotheses of sternum size allometry and the correlation of sternal shape with both size and locomotory capabilities, including flightlessness and the highly varying flight and swimming styles of Neornithes. Results: We find evidence for isometry of sternal size relative to body mass and document significant allometry of sternal shape alongside important correlations with locomotory capability, reflecting the effects of both body shape and musculoskeletal variation. Among these, we show that a large sternum with a deep or cranially projected sternal keel is necessary for powered flight in modern birds, that deeper sternal keels are correlated with slower but stronger flight, robust caudal sternal borders are associated with faster flapping styles, and that narrower sterna are associated with running abilities. Correlations between shape and locomotion are significant but show weak explanatory power, indicating that although sternal shape is broadly associated with locomotory ecology, other unexplored factors are also important. Conclusions: These results display the ecological importance of the avian sternum for flight and locomotion by providing a novel understanding of sternum form and function in Neornithes. Our study lays the groundwork for estimating the locomotory abilities of paravian dinosaurs, the ancestors to Neornithes, by highlighting the importance of this critical elem
... The logic of "evolutionary constraint" underlies the likelihood of homoplasy (Wake et al., 2011), and could explain the observed high frequency of craniofacial homoplasy across avian phylogeny (Klingenberg & Marugán-Lobón, 2013). Birds are also among the most encephalized vertebrates (Ksepka et al., 2020), and some birds, such as passerines and raptors, display a suite of traits that are comparable to those of primates, namely, domed cranial vaults, concavely flexed cranial bases, and retracted facial skeletons. Given the evolutionary importance of encephalization across vertebrates (Striedter, 2005), and that the tight coupling of brain and skull morphology is invariant and highly constrained (Young et al., 2014;Fabbri et al., 2017;Parsons et al., 2011), it is possible that the developmental pathways that structure skull evolution in mammals and birds are comparable. ...
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Birds exhibit an enormous variety of beak shapes. Such remarkable variation, however, has distracted research from other important aspects of their skull evolution, the nature of which has been little explored. Key aspects of avian skull variation appear to be qualitatively similar to those of mammals, encompassing variation in the degree of cranial vaulting, cranial base flexure, and the proportions and orientations of the occipital and facial regions. The evolution of these traits has been studied intensively in mammals under the Spatial Packing Hypothesis (SPH), an architectural constraint so‐called because the general anatomical organization and development of such skull parts makes them evolve predictably in response to changes in relative brain size. Such SPH predictions account for the different appearances of skull configurations across species, either in having longer or shorter faces, and caudally or ventrally oriented occiputs, respectively. This pattern has been morphometrically and experimentally proven in mammals but has not been examined in birds or other tetrapods, and so its generality remains unknown. We explored the SPH in an interspecific sample of birds using three‐dimensional geometric morphometrics. Our results show that the dominant trend of evolutionary variation in the skull of crown‐group birds can be predicted by the SPH, involving concomitant changes in the face, the cranial vault and the basicranium, and with striking similarities to craniofacial variation among mammals. Although craniofacial variation is significantly affected by allometry, these allometric effects are independent of the influence of the SPH on skull morphology, as are any effects of volumetric encephalization. Our results, therefore, validate the hypothesis that a general architectural constraint underlies skull homoplasy evolution of cranial morphology among avian clades, and possibly between birds and mammals, but they downplay encephalization and allometry as the only factors involved. We investigated the diversity of avian skull morphologies without the beak, testing the possible influence of relative brain size as it has been demostrated in mammals (so called Spatial Packing Hypothesis). We found a predictable and constrictive pattern of skull variation in which craniofacial arrangements (the orientation between the face, the cranial vault and the occiput) change at unison with relative brain size and cranial base length, strikingly similar to that of mammals.
... We were not able to quantify the influence of variation between datasets on comparative brain size model results here, due to non-independence of the datasets, but this would be a valuable focus for future work. Another important and related issue is that recent research suggests the relationship between brain and body size is often taxadependent [78,79]. Thus, the popular method of including body size as a covariate in models, in order to control for the relationship between brain and body size across a diverse range of species, may be flawed even when brain and body size estimates are accurate. ...
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There are multiple hypotheses for the evolution of cognition. The most prominent hypotheses are the Social Intelligence Hypothesis (SIH) and the Ecological Intelligence Hypothesis (EIH), which are often pitted against one another. These hypotheses tend to be tested using broad-scale comparative studies of brain size, where brain size is used as a proxy of cognitive ability, and various social and/or ecological variables are included as predictors. Here, we test how robust conclusions drawn from such analyses may be. First, we investigate variation in brain and body size measurements across >1000 bird species. We demonstrate that there is substantial variation in brain and body size estimates across datasets, indicating that conclusions drawn from comparative brain size models are likely to differ depending on the source of the data. Following this, we subset our data to the Corvides infraorder and interrogate how modelling decisions impact results. We show that model results change substantially depending on variable inclusion, source and classification. Indeed, we could have drawn multiple contradictory conclusions about the principal drivers of brain size evolution. These results reflect concerns from a growing number of researchers that conclusions drawn from comparative brain size studies may not be robust. We suggest that to interrogate hypotheses of cognitive evolution, a fruitful way forward is to focus on testing cognitive performance within and between closely related taxa, with an emphasis on understanding the relationship between informational uncertainty and cognitive evolution.
... These encephalization measures have been widely associated with behavioural and cognitive complexity (de Miguel & Henneberg, 1998;Jerison, 1973;Marino, 1998;Zollikofer & Ponce de León, 2013). In addition, recent analyses of variation in the allometric relationship between brain and body size across a variety of mammalian and avian clades have illuminated the macroevolutionary history of encephalization (Ksepka et al., 2020;Smaers et al., 2012;Weisbecker et al., 2021). Regardless of the comparative method used, choosing appropriate measures of both brain size and organismal size is critical for producing valid and interpretable encephalization measures (Hallgrímsson et al., 2019). ...
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Brain and skull tissues interact through molecular signalling and mechanical forces during head development, leading to a strong correlation between the neurocranium and the external brain surface. Therefore, when brain tissue is unavailable, neurocranial endocasts are often used to approximate brain size and shape. Evolutionary changes in brain morphology may have resulted in secondary changes to neurocranial morphology, but the developmental and genetic processes underlying this relationship are not well understood. Using automated phenotyping methods, we quantified the genetic basis of endocast variation across large genetically varied populations of laboratory mice in two ways: (1) to determine the contributions of various genetic factors to neurocranial form and (2) to help clarify whether a neurocranial variation is based on genetic variation that primarily impacts bone development or on genetic variation that primarily impacts brain development, leading to secondary changes in bone morphology. Our results indicate that endocast size is highly heritable and is primarily determined by additive genetic factors. In addition, a non‐additive inbreeding effect led to founder strains with lower neurocranial size, but relatively large brains compared to skull size; suggesting stronger canalization of brain size and/or a general allometric effect. Within an outbred sample of mice, we identified a locus on mouse chromosome 1 that is significantly associated with variation in several positively correlated endocast size measures. Because the protein‐coding genes at this locus have been previously associated with brain development and not with bone development, we propose that genetic variation at this locus leads primarily to variation in brain volume that secondarily leads to changes in neurocranial globularity. We identify a strain‐specific missense mutation within Akt3 that is a strong causal candidate for this genetic effect. Whilst it is not appropriate to generalize our hypothesis for this single locus to all other loci that also contribute to the complex trait of neurocranial skull morphology, our results further reveal the genetic basis of neurocranial variation and highlight the importance of the mechanical influence of brain growth in determining skull morphology. The genetic basis neurocranial size variation was analyzed in inbred and outbred mouse populations, indicating high heritability, with strong additive genetic contributions, as well as significant non‐additive contributions. A chromosome 1 locus encompassing protein‐coding genes of brain development is associated with several size measures, suggesting that genetic variation at this locus leads primarily to variation in brain volume that secondarily leads to changes in skull form.
... Our results also highlight the importance of considering differences in allometric slope and relaxing the assumption of shared allometric relationships for major taxonomic groups. With brain-body allometries, average slopes across major vertebrate taxonomic levels (class to genus) are relatively constant (Tsuboi et al., 2018); however, when not a priori defining grades based on strict taxonomic-level distinctions, significant differences in the allometric relationships of various groups at different taxonomic levels are readily detected (Ksepka et al., 2020;Smaers et al., 2021; Figure 3). Indeed, when we allow only intercept to vary between grades while assuming parallel slopes, we no longer detect any reliable grade shifts within actinopterygians. ...
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Brain region size generally scales allometrically with brain size, but mosaic shifts in brain region size independent of brain size have been found in several lineages and may be related to the evolution of behavioral novelty. African weakly electric fishes (Mormyroidea) evolved a mosaically enlarged cerebellum and hindbrain, yet the relationship to their behaviorally novel electrosensory system remains unclear. We addressed this by studying South American weakly electric fishes (Gymnotiformes) and weakly electric catfishes ( Synodontis spp.), which evolved varying aspects of electrosensory systems, independent of mormyroids. If the mormyroid mosaic increases are related to evolving an electrosensory system, we should find similar mosaic shifts in gymnotiforms and Synodontis . Using micro-computed tomography scans, we quantified brain region scaling for multiple electrogenic, electroreceptive, and non-electrosensing species. We found mosaic increases in cerebellum in all three electrogenic lineages relative to non-electric lineages and mosaic increases in torus semicircularis and hindbrain associated with the evolution of electrogenesis and electroreceptor type. These results show that evolving novel electrosensory systems is repeatedly and independently associated with changes in the sizes of individual major brain regions independent of brain size, suggesting that selection can impact structural brain composition to favor specific regions involved in novel behaviors.
... Great apes are the optimal living models of extinct hominins due to their behavioural, ecological, social, developmental, morphological and phylogenetic similarities (Duda & Zrzavý, 2013;Beran et al., 2016). The cognitive abilities of apes are mirrored by those of corvids (i.e., birds of the crow family) and parrots, despite their distant relatedness and different anatomynotably their brains (Olkowicz et al., 2016;Jacobs et al., 2019;Lambert et al., 2019;Ksepka et al., 2020). Australian raptors have been observed to pick up burning sticks and drop them elsewhere, which may cause more prey to flee that can be hunted (Bonta et al., 2017). ...
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Fire has substantially altered the course of human evolution. Cooking kindled brain expansion through improved energy and time budgets. However, little is known about the origins of fire use and its cognitive underpinnings (pyrocognition). Debates on how hominins innovated cooking focus on archaeological findings, but should also be informed by the response of animals towards heat sources. Here, we report six observations on two captive New Caledonian crows (Corvus moneduloides) contacting heat lamps with tools or placing raw food on them. The tools became singed or melted and the food had browned (and was removed). These results suggest that New Caledonian crows can use tools to investigate hot objects, which extends earlier findings that they use tools to examine potential hazards (pericular tool use), and place food on a heat source as play or exploration. Further research on animals will provide novel insights into the pyrocognitive origins of early humans.
... We then used a Bayesian multi-level model to extract species-level averages and standard errors (see the electronic supplementary material, methods). Brain mass was collected by A.I., from Iwaniuk et al. [39], from Schuck-Paim et al. [26] and from Ksepka et al. [40], and similarly to body size, we fitted a Bayesian multi-level model to extract species-level averages and standard errors. We also collected data for six additional potential explanatory variables, based on previously proposed causal relationships with life expectancy: diet (estimated protein content of main food items) [19], insularity (whether a species includes a continental range or not) [19], maximum latitudinal range (as a proxy for environmental variability) [9], clutch size [41], developmental time (from the start of incubation until fledging) and age of first possible reproduction (AFR) [18]. ...
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Previous studies have demonstrated a correlation between longevity and brain size in a variety of taxa. Little research has been devoted to understanding this link in parrots; yet parrots are well-known for both their exceptionally long lives and cognitive complexity. We employed a large-scale comparative analysis that investigated the influence of brain size and life-history variables on longevity in parrots. Specifically, we addressed two hypotheses for evolutionary drivers of longevity: the cognitive buffer hypothesis, which proposes that increased cognitive abilities enable longer lifespans, and the expensive brain hypothesis, which holds that increases in lifespan are caused by prolonged developmental time of, and increased parental investment in, large-brained offspring. We estimated life expectancy from detailed zoo records for 133 818 individuals across 244 parrot species. Using a principled Bayesian approach that addresses data uncertainty and imputation of missing values, we found a consistent correlation between relative brain size and life expectancy in parrots. This correlation was best explained by a direct effect of relative brain size. Notably, we found no effects of developmental time, clutch size or age at first reproduction. Our results suggest that selection for enhanced cognitive abilities in parrots has in turn promoted longer lifespans.
... Aside from regions and systems homologous to both clades, our understanding of the inner workings of the avian brain is limited relative to mammals, although a surge of research conducted over recent decades has made considerable progress in filling this gap (Reiner et al., 2004;Jarvis et al., 2005;Wada et al., 2017;Ksepka et al., 2020). Much of this work has focused on determining the functions of, and connectivity between, individual brain regions (see Cowan et al., 1961;Karten et al., 1973;Nottebohm et al., 1976;Wild et al., 1993;Shanahan et al., 2013 as examples). ...
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Social interaction among animals can occur under many contexts, such as during foraging. Our knowledge of the regions within an avian brain associated with social interaction is limited to the regions activated by a single context or sensory modality. We used 18F-fluorodeoxyglucose positron emission tomography (FDG-PET) to examine American crow ( Corvus brachyrhynchos ) brain activity in response to conditions associated with communal feeding. Using a paired approach, we exposed crows to either a visual stimulus (the sight of food), an audio stimulus (the sound of conspecifics vocalizing while foraging) or both audio/visual stimuli presented simultaneously and compared to their brain activity in response to a control stimulus (an empty stage). We found two regions, the nucleus taenia of the amygdala (TnA) and a medial portion of the caudal nidopallium, that showed increased activity in response to the multimodal combination of stimuli but not in response to either stimulus when presented unimodally. We also found significantly increased activity in the lateral septum and medially within the nidopallium in response to both the audio-only and the combined audio/visual stimuli. We did not find any differences in activation in response to the visual stimulus by itself. We discuss how these regions may be involved in the processing of multimodal stimuli in the context of social interaction.
... New Caledonian Crow (Corvus moneduloides) is a species of Corvidae in Passeriformes that exhibits tool-using behavior in the wild (Hunt, 1996;Matsui et al., 2016), and has a larger brain compared to those of other species in Passeriformes (Cnotka et al., 2008). Overington et al. (2009) found a positive relationship between innovativeness in foraging technique and brain size in 76 avian families and supported the hypothesis that large brains allow for the production of novel behavior patterns (Ksepka et al., 2020;Lefebvre & Bolhuis, 2003). ...
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Studies have suggested that the brain morphology and flight ability of Aves are interrelated; however, such a relationship has not been thoroughly investigated. This study aimed to examine whether flight ability, volant or flightless, affects brain morphology (size and shape) in the Rallidae, which has independently evolved to adapt secondary flightlessness multiple times within a single taxonomic group. Brain endocasts were extracted from computed tomography images of the crania, measured by 3D geometric morphometrics, and were analyzed using principal component analysis. The results of phylogenetic ANCOVA showed that flightless rails have brain sizes and shapes that are significantly larger than and different from those of volant rails, even after considering the effects of body mass and brain size respectively. Flightless rails tended to have a wider telencephalon and more inferiorly positioned foramen magnum than volant rails. Although the brain is an organ that requires a large amount of metabolic energy, reduced selective pressure for a lower body weight may have allowed flightless rails to have larger brains. The evolution of flightlessness may have changed the position of the foramen magnum downward, which would have allowed the support of the heavier cranium. The larger brain may have facilitated the acquisition of cognitively advanced behavior, such as tool‐using behavior, among rails. Flightless rails have brain sizes and shapes that are significantly larger than and different from those of volant rails. Flightless rails tended to have a wider telencephalon and more inferiorly positioned foramen magnum than volant rails. The larger brain may have facilitated the acquisition of cognitively advanced behavior, such as tool‐using behavior, among rails.
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The rich early fossil record of the echinoderms reveals surprisingly dynamic patterns of body plan evolution and suggests that currently popular theories about how the major features of the animal originated and were maintained are unlikely to be correct.
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Niche expansion is a critical step in the speciation process. Large brains linked to improved cognitive ability may enable species to expand their niches and forage in new ways, thereby promoting speciation. Despite considerable work on ecological divergence in brain size and its importance in speciation, relatively little is known about how brain shape relates to behavioral, ecological, and taxonomic diversity at macroevolutionary scales. This is due in part to inherent challenges with quantifying brain shape across many species. Here we present a novel, semiautomated approach for rapidly phenotyping brain shape using semilandmarks derived from X-ray computed microtomography scans. We then test its utility by parsing evolutionary trends within a diverse radiation of birds: kingfishers (Aves: Alcedinidae). Multivariate comparative analyses reveal that rates of brain shape evolution (but not beak shape) are positively correlated with lineage diversification rates. Distinct brain shapes are further associated with changes in body size and foraging behavior, suggesting both allometric and ecological constraints on brain shape evolution. These results are in line with the idea of brains acting as a "master regulator" of critical processes governing speciation, such as dispersal, foraging behavior, and dietary niche.
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Red Junglefowl ( Gallus gallus ) were selected for divergent levels of fear of humans during eight generations, causing the selection lines to differ in fear levels as well as in the proportional brain and cerebellum masses. Birds from the two lines were then crossed to obtain an F3 intercross in order to study the correlations between brain mass and fear learning. We exposed 105 F3-animals individually to a fear habituation and memory test at 8 days of age, where the reactions to repeated light flashes were assessed on 2 consecutive days. After culling, the absolute and relative sizes of each of four brain regions were measured. Stepwise regression was used to analyse the effects of the size of each brain region on habituation and memory. There were no effects of any brain region on the habituation on day one. However, birds with a larger absolute size of cerebellum had significantly reduced reactions to the fearful stimuli on day two, indicating a better memory of the stimuli. No other regions had significant effects. We conclude that increased cerebellum size may have been important in facilitating chicken domestication, allowing them to adapt to a life with humans.
Chapter
Our understanding of the early evolution of birds has advanced over the past 2 decades, thanks to an ever-improving fossil record. Extraordinary fossils have revealed new details about the evolution of the avian brain, respiratory system, digestive tract, and reproductive system. Many of the traits most strongly associated with birds first arose in nonavian theropod dinosaurs. Theropods evolved pennaceous feathers, incipient wings, and gliding flight long before modern birds appeared. Birds likewise inherited features such as an expanded forebrain, gizzard, dorsally immobile lung, pigmented eggs, and paternal brooding system from their theropod ancestors. Yet, the earliest birds also retained primitive traits such as teeth, clawed hands, long bony tails, partially buried nests, and slower growth. The evolution of birds was profoundly influence by the Cretaceous–Paleogene mass extinction, which wiped out the previously dominant Enantiornithines (“opposite birds”). This sets the stage for modern birds to radiate into the most diverse major clade of tetrapods.
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Why do some species occur in small, restricted areas, while others are distributed globally? Environmental heterogeneity increases with area and so does the number of species. Hence, diverse biotic and abiotic conditions across large ranges may lead to specific adaptations that are often linked to a species' genome size and chromosome number. Therefore, a positive association between genome size and geographic range is anticipated. Moreover, high cognitive ability in organisms would be favored by natural selection to cope with the dynamic conditions within large geographic ranges. Here, we tested these hypotheses in birds-the most mobile terrestrial vertebrates-and accounted for the effects of various confounding variables, such as body mass, relative brain mass, and geographic latitude. Using phylogenetic generalized least squares and phylogenetic confirmatory path analysis, we demonstrated that range size is positively associated with bird genome size but probably not with chromosome number. Moreover, relative brain mass had no effect on range size, whereas body mass had a possible weak and negative effect, and range size was larger at higher geographic latitudes. However, our models did not fully explain the overall variation in range size. Hence, natural selection may impose larger genomes in birds with larger geographic ranges, although there may be additional explanations for this phenomenon.
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Birds have acute vision and many remarkable visual cognition abilities, due to their unique living environment. The underlying neural mechanisms have also attracted interests of researchers in neuroscience. Here, we firstly summarize the visual cognition abilities of birds, and make a comparison with mammals. Secondly, the underlying neural mechanisms are presented, including histological structure of avian brain and visual pathways, typical experimental results and conclusions in electrochemistry and electrophysiology. The latter mainly focuses on several higher brain areas related to visual cognition, including mesopallium ventrolaterale, entopallium, visual Wulst, and nidopallium caudolaterale. Finally, we make a conclusion and provide a suggestion about future studies on revealing the neural mechanisms of avian visual cognition. This review presents a detailed understanding of avian visual cognition and would be helpful in ornithology studies in the field of cognitive neuroscience.
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There are multiple hypotheses for the evolution of cognition. The most prominent hypotheses are the Social Intelligence Hypothesis (SIH) and the Ecological Intelligence Hypothesis (EIH), which are often pitted against one another. These hypotheses tend to be tested using broad-scale comparative studies of brain size, where brain size is used as a proxy of cognitive ability, and various social and/or ecological variables are included as predictors. Here, we test how methodologically robust such analyses are. First, we investigate variation in brain and body size measurements across >1000 species of bird. We demonstrate that there is substantial variation in brain and body size estimates across datasets, indicating that conclusions drawn from comparative brain size models are likely to differ depending on the source of the data. Following this, we subset our data to the Corvides infraorder and interrogate how modelling decisions impact results. We show that model results change substantially depending on variable inclusion, source and classification. Indeed, we could have drawn multiple contradictory conclusions about the principal drivers of brain size evolution. These results reflect recent concerns that current methods in comparative brain size studies are not robust. We add our voices to a growing community of researchers suggesting that we move on from using such methods to investigate cognitive evolution. We suggest that a more fruitful way forward is to instead use direct measures of cognitive performance to interrogate why variation in cognition arises within species and between closely related taxa.
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Despite a considerable interest of researchers to the issue of variation in skull shapes of birds and factors influencing it, some drivers associated with the design features of an entire bird body, which are important for both successful terrestrial locomotion and flight, are overlooked. One of such factors, in our opinion, is relative skull size (skull length in relation to body mass), which can affect the position of the body's center of gravity. We tested effects of relative skull size, allometry (i.e. absolute skull size), and diet on variation in skull shape. The study was conducted on 50 songbird species with a wide range of body mass (8.3g to 570g) and dietary preferences (granivores, insectivores/granivores, insectivores, omnivores). Skull shape was analyzed using 2D geometric morphometrics. We revealed that similar patterns of skull shape occur among passerines with different body sizes and diets. The relative skull size predicted skull shape to a similar extent and with a similar pattern as the absolute size. In our opinion, the effect of the relative skull size on skull shape variation is likely due to biomechanical constraints related to flight.
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Variation in neocortex size is one of the defining features of mammalian brain evolution. The paramount assumption has been that neocortex size indicates a monotonic allometric relationship with brain size. This assumption holds the concomitant neurodevelopmental assumption that the ontogenetic trajectory of neocortex size is so stable across species that it restrains changes in the direction of evolution. Here we test this fundamental assumption. Whereas previous research has focused exclusively on changes in mean size among groups (i.e., intercept), we additionally investigate changes in covariation (i.e., slope) and strength of allometric integration (i.e., residual variation). We further increase data resolution by investigating 350 species representing 11 mammalian orders. Results identify nine shifts in covariation between neocortex and brainstem in different mammalian groups, indicate that these shifts occur independently of shifts in size, and demonstrate that the strength of allometric integration across different neocortical regions in primates is inversely related to the neurodevelopmental gradient such that later developing regions underwent more evolutionary change. Although our results confirm that variation in brain organization is structured along a neurodevelopmental gradient, our results suggest two additional principles of size reorganization in brain evolution: (1) repatterning of growth allocation among brain regions may occur independently of size and (2) later developing regions indicate faster evolution, not necessarily directional evolution toward larger size. We conclude that the evolution of neocortex size in mammals is far more variable than previously assumed, in turn suggesting a higher degree of evolutionary flexibility in neurodevelopmental patterning than commonly suggested.
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Comparative variation in brain size is arguably one of the most dominant features of primate evolution. Enduring questions in this context comprise whether evolutionary changes in certain brain regions outpace changes in other regions, and to what extent such regional variation between species explains comparative variation in overall brain size. To answer this question, we investigate the tempo and mode of evolution of brain organization using the largest combination of brain regions and species analyzed to date (36 brain regions, together representing over 90% of overall brain size, across 17 anthropoid primates, including humans). Following studies suggesting that the expansion of the major constituent regions of the cortico-cerebellar system (CCS) predominantly explain human brain size expansion, we test whether the link between variation in the CCS and brain size is consistent across primates. Results indicate that the constituent brain regions of the CCS show the highest rates of evolution, demonstrate a significant modular pattern of evolution, and closely align with changes in overall brain size. This phenotypic structure is consistent across different taxonomic scales, suggesting that the evolution of anthropoid brain organization is underpinned by a stable genetic structure and is characterized by a conserved evolutionary trajectory towards the CCS. Results hereby suggest that the expansion of the CCS is the primary driver of brain expansion in anthropoid primates. These findings have fundamental implications for our understanding of the nature of primate and human cognition, and the genetic and developmental structure that underpins brain evolution.
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The allometric relationship between brain and body size among vertebrates is often considered a manifestation of evolutionary constraints. However, birds and mammals have undergone remarkable encephalization, in which brain size has increased without corresponding changes in body size. Here, we explore the hypothesis that a reduction of phenotypic integration between brain and body size has facilitated encephalization in birds and mammals. Using a large dataset comprising 20,213 specimens across 4,587 species of jawed vertebrates, we show that the among-species (evolutionary) brain-body allometries are remarkably constant, both across vertebrate classes and across taxonomic levels. Birds and mammals, however, are exceptional in that their within-species (static) allometries are shallower and more variable than in other vertebrates. These patterns are consistent with the idea that birds and mammals have reduced allometric constraints that are otherwise ubiquitous across jawed vertebrates. Further exploration of ontogenetic allometries in selected taxa of birds, fishes and mammals reveals that birds and mammals have extended the period of fetal brain growth compared to fishes. Based on these findings, we propose that avian and mammalian encephalization has been contingent on increased variability in brain growth patterns.
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Theory and evidence suggest that some selective pressures are more common on islands than in adjacent mainland habitats, leading evolution to follow predictable trends. The existence of predictable evolutionary trends has nonetheless been difficult to demonstrate, mainly because of the challenge of separating in situ evolution from sorting processes derived from colonization events. Here we use brain size measurements of >1900 avian species to reveal the existence of one such trend: increased brain size in island dwellers. Based on sister-taxa comparisons and phylogenetic ancestral trait estimations, we show that species living on islands have relatively larger brains than their mainland relatives and that these differences mainly reflect in situ evolution rather than varying colonization success. Our findings reinforce the view that in some instances evolution may be predictable, and yield insight into why some animals evolve larger brains despite substantial energetic and developmental costs.
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Comparative studies tend to differ from optimality and functionality studies in how they treat adaptation. While the comparative approach focuses on the origin and change of traits, optimality studies assume that adaptations are maintained at an optimum by stabilizing selection. This paper presents a model of adaptive evolution on a macroevolutionary time scale that includes the maintenance of traits at adaptive optima by stabilizing selection as the dominant evolutionary force. Interspecific variation is treated as variation in the position of adaptive optima. The model illustrates how phylogenetic constraints not only lead to correlations between phylogenetically related species, but also to imperfect adaptations. From this model, a statistical comparative method is derived that can be used to estimate the effect of a selective factor on adaptive optima in a way that would be consistent with an optimality study of adaptation to this factor. The method is illustrated with an analysis of dental evolution in fossil horses. The use of comparative methods to study evolutionary trends is also discussed.
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Endocasts are windows into deep history and as such provide modern neuroscience a more complete appreciation of: (1) the brain's evolutionary potential (by allowing sampling of extinct lineages) and (2) the origins of modern neurological disparity. Imaging technology has increased the number of endocasts and thus their integrative potential for informing broad patterns of brain evolution. Our goal is to facilitate this integration by explicating the inferential framework in which endocasts are studied, their anatomical identity, and the hypotheses they can and cannot address. Examples of endocasts' explanatory power and limitations are drawn largely from birds and their extinct relatives.
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Environmental variability has long been postulated as a major selective force in the evolution of large brains. However, assembling evidence for this hypothesis has proved difficult. Here, by combining brain size information for over 1,200 bird species with remote-sensing analyses to estimate temporal variation in ecosystem productivity, we show that larger brains (relative to body size) are more likely to occur in species exposed to larger environmental variation throughout their geographic range. Our reconstructions of evolutionary trajectories are consistent with the hypothesis that larger brains (relative to body size) evolved when the species invaded more seasonal regions. However, the alternative—that the species already possessed larger brains when they invaded more seasonal regions—cannot be completely ruled out. Regardless of the exact mechanism, our findings provide strong empirical support for the association between large brains and environmental variability.
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Some birds achieve primate-like levels of cognition, even though their brains tend to be much smaller in absolute size. This poses a fundamental problem in comparative and computational neuroscience, because small brains are expected to have a lower information-processing capacity. Using the isotropic fractionator to determine numbers of neurons in specific brain regions, here we show that the brains of parrots and songbirds contain on average twice as many neurons as primate brains of the same mass, indicating that avian brains have higher neuron packing densities than mammalian brains. Additionally, corvids and parrots have much higher proportions of brain neurons located in the pallial telencephalon compared with primates or other mammals and birds. Thus, large-brained parrots and corvids have forebrain neuron counts equal to or greater than primates with much larger brains. We suggest that the large numbers of neurons concentrated in high densities in the telencephalon substantially contribute to the neural basis of avian intelligence.
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Phylogenetic generalized least squares (PGLS) has become one of the most commonly used phylogenetic comparative methods. Despite its common use, descriptions and applications of methods to test for species' deviations from allometric predictions using phylogenetic regression have been piecemeal. We simplify previous computational descriptions of PGLS standard errors in a manner that can be easily generalized towards more complex general linear models. We focus on the implementation of phylogenetic analysis of covariance, which provides a direct test for the equality of intercepts and slopes. Our computational descriptions allow testing whether individual species, or a group of species, deviate significantly from allometric predictions. The use of PGLS confidence and prediction intervals and phylogenetic analysis of covariance is exemplified in an analysis of brain structure volumes in primates. This article is protected by copyright. All rights reserved.
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Understanding the mechanisms of evolution of brain pathways for complex behaviours is still in its infancy. Making further advances requires a deeper understanding of brain homologies, novelties and analogies. It also requires an understanding of how adaptive genetic modifications lead to restructuring of the brain. Recent advances in genomic and molecular biology techniques applied to brain research have provided exciting insights into how complex behaviours are shaped by selection of novel brain pathways and functions of the nervous system. Here, we review and further develop some insights to a new hypothesis on one mechanism that may contribute to nervous system evolution, in particular by brain pathway duplication. Like gene duplication, we propose that whole brain pathways can duplicate and the duplicated pathway diverge to take on new functions. We suggest that one mechanism of brain pathway duplication could be through gene duplication, although other mechanisms are possible. We focus on brain pathways for vocal learning and spoken language in song-learning birds and humans as example systems. This view presents a new framework for future research in our understanding of brain evolution and novel behavioural traits.
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Living birds constitute the only vertebrate group whose brain volume relative to body size approaches the uniquely expanded values expressed by mammals. The broad suite of complex behaviors exhibited by crown-group birds, including sociality, vocal learning, parental care, and flying, suggests the origins of their encephalization was likely driven by a mosaic of selective pressures. If true, the historical pattern of brain expansion may be more complex than either a gradual expansion, as proposed by early studies of the avian brain, or a sudden expansion correlating with the appearance of flight. The origins of modern avian neuroanatomy are obscured by the more than 100 million years of evolution along their phylogenetic stem (from the origin of the modern radiation in the Middle Jurassic to the split from crocodile-line archosaurs). Here we use phylogenetic comparative approaches to explore which evolutionary scenarios best explain variation in measured volumes of digitally partitioned endocasts of modern birds and their non-avian ancestors. Our analyses suggest that variation in the relative volumes of the endocranium and cerebrum explain most of the structural variation in this lineage. Generalized multi-regime Ornstein-Uhlenbeck (OU) models suggest that powered flight does not appear to be a driver of observed variation, reinforcing the hypothesis that the deep history of the avian brain is complex, with nuances still to be discovered.
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Although reconstruction of the phylogeny of living birds has progressed tremendously in the last decade, the evolutionary history of Neoaves-a clade that encompasses nearly all living bird species-remains the greatest unresolved challenge in dinosaur systematics. Here we investigate avian phylogeny with an unprecedented scale of data: >390,000 bases of genomic sequence data from each of 198 species of living birds, representing all major avian lineages, and two crocodilian outgroups. Sequence data were collected using anchored hybrid enrichment, yielding 259 nuclear loci with an average length of 1,523 bases for a total data set of over 7.8 × 10(7) bases. Bayesian and maximum likelihood analyses yielded highly supported and nearly identical phylogenetic trees for all major avian lineages. Five major clades form successive sister groups to the rest of Neoaves: (1) a clade including nightjars, other caprimulgiforms, swifts, and hummingbirds; (2) a clade uniting cuckoos, bustards, and turacos with pigeons, mesites, and sandgrouse; (3) cranes and their relatives; (4) a comprehensive waterbird clade, including all diving, wading, and shorebirds; and (5) a comprehensive landbird clade with the enigmatic hoatzin (Opisthocomus hoazin) as the sister group to the rest. Neither of the two main, recently proposed Neoavian clades-Columbea and Passerea-were supported as monophyletic. The results of our divergence time analyses are congruent with the palaeontological record, supporting a major radiation of crown birds in the wake of the Cretaceous-Palaeogene (K-Pg) mass extinction.
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The rapidly expanding interest in, and availability of, digital tomography data to visualize casts of the vertebrate endocranial cavity housing the brain (endocasts) presents new opportunities and challenges to the field of comparative neuroanatomy. The opportunities are many, ranging from the relatively rapid acquisition of data to the unprecedented ability to integrate critically important fossil taxa. The challenges consist of navigating the logistical barriers that often separate a researcher from high-quality data and minimizing the amount of non-biological variation expressed in endocasts – variation that may confound meaningful and synthetic results. Our purpose here is to outline preferred approaches for acquiring digital tomographic data, converting those data to an endocast, and making those endocasts as meaningful as possible when considered in a comparative context. This review is intended to benefit those just getting started in the field but also serves to initiate further discussion between active endocast researchers regarding the best practices for advancing the discipline. Congruent with the theme of this volume, we draw our examples from birds and the highly encephalized non-avian dinosaurs that comprise closely related outgroups along their phylogenetic stem lineage.
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The comparative anatomy of sensory systems has played a major role in developing theories and principles central to evolutionary neuroscience. This includes the central tenet of many comparative studies, the principle of proper mass, which states that the size of a neural structure reflects its processing capacity. The size of structures within the sensory system is not, however, the only salient variable in sensory evolution. Further, the evolution of the brain and behavior are intimately tied to phylogenetic history, requiring studies to integrate neuroanatomy with behavior and phylogeny to gain a more holistic view of brain evolution. Birds have proven to be a useful group for these studies because of widespread interest in their phylogenetic relationships and a wealth of information on the functional organization of most of their sensory pathways. In this review, we examine the principle of proper mass in relation differences in the sensory capabilities among birds. We discuss how neuroanatomy, behavior, and phylogeny can be integrated to understand the evolution of sensory systems in birds providing evidence from visual, auditory, and somatosensory systems. We also consider the concept of a "trade-off," whereby one sensory system (or subpathway within a sensory system), may be expanded in size, at the expense of others, which are reduced in size.
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The ability to imitate complex sounds is rare, and among birds has been found only in parrots, songbirds, and hummingbirds. Parrots exhibit the most advanced vocal mimicry among non-human animals. A few studies have noted differences in connectivity, brain position and shape in the vocal learning systems of parrots relative to songbirds and hummingbirds. However, only one parrot species, the budgerigar, has been examined and no differences in the presence of song system structures were found with other avian vocal learners. Motivated by questions of whether there are important differences in the vocal systems of parrots relative to other vocal learners, we used specialized constitutive gene expression, singing-driven gene expression, and neural connectivity tracing experiments to further characterize the song system of budgerigars and/or other parrots. We found that the parrot brain uniquely contains a song system within a song system. The parrot "core" song system is similar to the song systems of songbirds and hummingbirds, whereas the "shell" song system is unique to parrots. The core with only rudimentary shell regions were found in the New Zealand kea, representing one of the only living species at a basal divergence with all other parrots, implying that parrots evolved vocal learning systems at least 29 million years ago. Relative size differences in the core and shell regions occur among species, which we suggest could be related to species differences in vocal and cognitive abilities.
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Coelurosauria is the most diverse clade of theropod dinosaurs. Much of this diversity is present in Paraves—the clade of dinosaurs containing dromaeosaurids, troodontids, and avialans. Paraves has over 160 million years of evolutionary history that continues to the present day. The clade represents the most diverse living tetrapod group (there are over 9000 extant species of Aves—a word used here as synonomous with “bird”), and it is at the root of the paravian radiation, when dromaeosaurids, troodontids, and avialans were diverging from one another, that we find the morphology and soft tissue changes associated with the origin of modern avian flight. Within the first 15 million years of known paravian evolutionary history members of this clade exhibited a difference of nearly four orders of magnitude in body size, a value that is similar to the extreme body size disparity present today in mammalian carnivorans, avians, and varanoid squamates. In this respect, Paraves is an important case study in characterizing the patterns, processes, and dynamics of evolutionary size change. This last point is of particular interest because of the historical significance placed on the role of body size reduction in the origin of powered avian flight.Our study reviews and revises the membership of Dromaeosauridae and provides an apomorphy-based diagnosis for all valid taxa. Of the currently 31 named dromaeosaurid species, we found 26 to be valid. We provide the most detailed and comprehensive phylogenetic analysis of paravians to date in order to explore the phylogenetic history of dromaeosaurid taxa. The general pattern of paravian relationships is explored within the broader context of Coelurosauria with an emphasis on sampling basal avialans, because of their importance for character optimizations at the base of Paraves.A large dataset was constructed by merging two datasets, one examining coelurosaur relationships broadly (based on previous TWiG datasets) and the other examining avialan relationships specifically (Clarke et al., 2006). This merged dataset was then significantly revised and supplemented with novel character analysis focusing on paravian taxa. During character analysis, particular attention was given to basal members of Dromaeosauridae, enigmatic basal paravians such as Jinfengopteryx elegans and Anchiornis huxleyi, and the incorporation of new morphological information from two undescribed troodontid species from the Late Cretaceous of Mongolia. A final dataset of 474 characters scored for 111 taxa was used to address paravian evolution. This dataset is important in that it bridges a phylogenetic gap that had persisted between studies on birds and studies on all other coelurosaurs. Most scorings in this matrix were based on the direct observation of specimens.All most parsimonious trees recovered in the cladistic analysis support the monophyly of Paraves, Troodontidae, Dromaeosauridae, and Deinonychosauria. A new clade of basal troodontids is discovered including two undescribed Mongolian troodontids and Jinfengopteryx elegans. Xiaotingia and Anchiornis form a clade at the base of Troodontidae. Recently proposed relationships within Dromaeosauridae are further supported and a succession of clades from Gondwana and Asia form sister taxa to a clade of Laurasian dromaeosaurids. Avialan monophyly is strongly supported with Archaeopteryx, Sapeornis, Jeholornis, and Jixiangornis forming the successive sister taxa to the Confuciusornis node. This topology supports a more basal position for Sapeornis than previous phylogenetic analyses and indicates a progressive acquisition of a fully “avian” shoulder morphology.
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To better determine the history of modern birds, we performed a genome-scale phylogenetic analysis of 48 species representing all orders of Neoaves using phylogenomic methods created to handle genome-scale data. We recovered a highly resolved tree that confirms previously controversial sister or close relationships. We identified the first divergence in Neoaves, two groups we named Passerea and Columbea, representing independent lineages of diverse and convergently evolved land and water bird species. Among Passerea, we infer the common ancestor of core landbirds to have been an apex predator and confirm independent gains of vocal learning. Among Columbea, we identify pigeons and flamingoes as belonging to sister clades. Even with whole genomes, some of the earliest branches in Neoaves proved challenging to resolve, which was best explained by massive protein-coding sequence convergence and high levels of incomplete lineage sorting that occurred during a rapid radiation after the Cretaceous-Paleogene mass extinction event about 66 million years ago. Copyright © 2014, American Association for the Advancement of Science.
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Our understanding of macroevolutionary patterns of adaptive evolution has greatly increased with the advent of large-scale phylogenetic comparative methods. Widely used Ornstein–Uhlenbeck (OU) models can describe an adaptive process of divergence and selection. However, inference of the dynamics of adaptive landscapes from comparative data is complicated by interpretational difficulties, lack of identifiability among parameter values and the common requirement that adaptive hypotheses must be assigned a priori. Here, we develop a reversible-jump Bayesian method of fitting multi-optima OU models to phylogenetic comparative data that estimates the placement and magnitude of adaptive shifts directly from the data. We show how biologically informed hypotheses can be tested against this inferred posterior of shift locations using Bayes Factors to establish whether our a priori models adequately describe the dynamics of adaptive peak shifts. Furthermore, we show how the inclusion of informative priors can be used to restrict models to biologically realistic parameter space and test particular biological interpretations of evolutionary models. We argue that Bayesian model fitting of OU models to comparative data provides a framework for integrating of multiple sources of biological data—such as microevolutionary estimates of selection parameters and paleontological timeseries—allowing inference of adaptive landscape dynamics with explicit, process-based biological interpretations.
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Recent discoveries have highlighted the dramatic evolutionary transformation of massive, ground-dwelling theropod dinosaurs into light, volant birds. Here, we apply Bayesian approaches (originally developed for inferring geographic spread and rates of molecular evolution in viruses) in a different context: to infer size changes and rates of anatomical innovation (across up to 1549 skeletal characters) in fossils. These approaches identify two drivers underlying the dinosaur-bird transition. The theropod lineage directly ancestral to birds undergoes sustained miniaturization across 50 million years and at least 12 consecutive branches (internodes) and evolves skeletal adaptations four times faster than other dinosaurs. The distinct, prolonged phase of miniaturization along the bird stem would have facilitated the evolution of many novelties associated with small body size, such as reorientation of body mass, increased aerial ability, and paedomorphic skulls with reduced snouts but enlarged eyes and brains.
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Phylogenies are increasingly used in all fields of medical and biological research. Moreover, because of the next generation sequencing revolution, datasets used for conducting phylogenetic analyses grow at an unprecedented pace. RAxML (Randomized Axelerated Maximum Likelihood) is a popular program for phylogenetic analyses of large datasets under maximum likelihood. Since the last RAxML paper in 2006, it has been continuously maintained and extended to accommodate the increasingly growing input datasets and to serve the needs of the user community. I present some of the most notable new features and extensions of RAxML, such as, a substantial extension of substitution models and supported data types, the introduction of SSE3, AVX, and AVX2 vector intrinsics, techniques for reducing the memory requirements of the code and a plethora of operations for conducting post-analyses on sets of trees. In addition, an up-to-date, 50 page user manual covering all new RAxML options is available. The code is available under GNU GPL at https://github.com/stamatak/standard-RAxML. Alexandros.Stamatakis@h-its.org.
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Many questions in evolutionary biology require the quantification and comparison of rates of phenotypic evolution. Recently, phylogenetic comparative methods have been developed for comparing evolutionary rates on a phylogeny for single, univariate traits (σ(2)), and evolutionary rate matrices (R) for sets of traits treated simultaneously. However, high-dimensional traits like shape remain under-examined with this framework, because methods suited for such data have not been fully developed. In this article, I describe a method to quantify phylogenetic evolutionary rates for high-dimensional multivariate data (σ(2)mult), found from the equivalency between statistical methods based on covariance matrices and those based on distance matrices (R-mode and Q-mode methods). I then use simulations to evaluate the statistical performance of hypothesis testing procedures that compare σ(2)mult for two or more groups of species on a phylogeny. Under both isotropic and non-isotropic conditions, and for differing numbers of trait dimensions, the proposed method displays appropriate Type I error and high statistical power for detecting known differences in σ(2)mult among groups. By contrast, the Type I error rate of likelihood tests based on the evolutionary rate matrix (R) increases as the number of trait dimensions (p) increases, and becomes unacceptably large when only a few trait dimensions are considered. Further, likelihood tests based on R cannot be computed when the number of trait dimensions equals or exceeds the number of taxa in the phylogeny (i.e., when p ≥ N). These results demonstrate that tests based on σ(2)mult provide a useful means of comparing evolutionary rates for high-dimensional data that are otherwise not analytically accessible to methods based on the evolutionary rate matrix. This advance thus expands the phylogenetic comparative toolkit for high-dimensional phenotypic traits like shape. Finally, I illustrate the utility of the new approach by evaluating rates of head shape evolution in a lineage of Plethodon salamanders.
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Scaling relationships between skeletal dimensions and body mass in extant birds are often used to estimate body mass in fossil crown-group birds, as well as in stem-group avialans. However, useful statistical measurements for constraining the precision and accuracy of fossil mass estimates are rarely provided, which prevents the quantification of robust upper and lower bound body mass estimates for fossils. Here, we generate thirteen body mass correlations and associated measures of statistical robustness using a sample of 863 extant flying birds. By providing robust body mass regressions with upper- and lower-bound prediction intervals for individual skeletal elements, we address the longstanding problem of body mass estimation for highly fragmentary fossil birds. We demonstrate that the most precise proxy for estimating body mass in the overall dataset, measured both as coefficient determination of ordinary least squares regression and percent prediction error, is the maximum diameter of the coracoid's humeral articulation facet (the glenoid). We further demonstrate that this result is consistent among the majority of investigated avian orders (10 out of 18). As a result, we suggest that, in the majority of cases, this proxy may provide the most accurate estimates of body mass for volant fossil birds. Additionally, by presenting statistical measurements of body mass prediction error for thirteen different body mass regressions, this study provides a much-needed quantitative framework for the accurate estimation of body mass and associated ecological correlates in fossil birds. The application of these regressions will enhance the precision and robustness of many mass-based inferences in future paleornithological studies.
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Morphological traits often covary within and among species according to simple power laws referred to as allometry. Such allometric relationships may result from common growth regulation, and this has given rise to the hypothesis that allometric exponents may have low evolvability and constrain trait evolution. We formalize hypotheses for how allometry may constrain morphological trait evolution across taxa, and test these using more than three-hundred empirical estimates of static (within-species) allometric relations of animal morphological traits. Although we find evidence for evolutionary changes in allometric parameters on million-year, cross-species time scales, there is limited evidence for microevolutionary changes in allometric slopes. Accordingly, we find that static allometries often predict evolutionary allometries on the subspecies level, but less so across species. Although there is a large body of work on allometry in a broad sense that includes all kinds of morphological trait-size relationships, we found relatively little information about the evolution of allometry in the narrow sense of a power relationship. Despite the many claims of microevolutionary changes of static allometries in the literature, hardly any of these apply to narrow-sense allometry, and we argue that the hypothesis of strongly constrained static allometric slopes remains viable. This article is protected by copyright. All rights reserved.
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Features that were once considered exclusive to modern birds, such as feathers and a furcula, are now known to have first appeared in non-avian dinosaurs. However, relatively little is known of the early evolutionary history of the hyperinflated brain that distinguishes birds from other living reptiles and provides the important neurological capablities required by flight. Here we use high-resolution computed tomography to estimate and compare cranial volumes of extant birds, the early avialan Archaeopteryx lithographica, and a number of non-avian maniraptoran dinosaurs that are phylogenetically close to the origins of both Avialae and avian flight. Previous work established that avian cerebral expansion began early in theropod history and that the cranial cavity of Archaeopteryx was volumetrically intermediate between these early forms and modern birds. Our new data indicate that the relative size of the cranial cavity of Archaeopteryx is reflective of a more generalized maniraptoran volumetric signature and in several instances is actually smaller than that of other non-avian dinosaurs. Thus, bird-like encephalization indices evolved multiple times, supporting the conclusion that if Archaeopteryx had the neurological capabilities required of flight, so did at least some other non-avian maniraptorans. This is congruent with recent findings that avialans were not unique among maniraptorans in their ability to fly in some form.
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Body size is a crucial life history parameter for an organism. Therefore, mass estimation for fossil species is important for many kinds of analyses. Several attempts have been made to yield equations applicable to dinosaurs. In this paper, we offer bi- and multivariate equations based on log transformed appendicular skeleton data from a sample of 16 theropods which were known from reasonably complete skeletal remains, and spanning a wide size range. Body masses of the included taxa had been found by displacement methods of scale models, based on measurements taken directly on the mounted skeletons. Seven of the bivariate regression analyses resulted in correlation coefficients equal to or above 0.975 and femoral length was the best available measurement (r=0.995; standard error of the estimate (%SEE)=19.26; percent prediction error (). Also, 32 multivariate analyses yielded equations with high correlation coefficients (r>0.990) and low standard errors.
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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.
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Endocranial volumes of vertebrate skulls and brain masses are often used interchangeably in comparative analyses of brain size. We test whether endocranial volume can be used as a reliable estimate of brain size in birds by comparing endocranial volumes with brain masses across 82 species using absolute values and with respect to body size. The results of paired tests across all 82 species and within two orders, Passeriformes and Psittaciformes, did not yield a significant difference between the two measures. These results were supported by correlational analyses that showed a significant positive relationship between endocranial volume and brain mass. Unpaired tests within short-tailed shearwaters (Puffinus tenuirostris) and paired tests within budgerigars (Melopsittacus undulatus) also yielded no significant differences between endocranial volume and brain mass. Thus, a combination of interspecific and intraspecific comparisons indicates that endocranial volume does provide a reliable estimate of brain size. Although this may enable more rapid collection of avian brain size data, endocranial volume should be used with caution because it cannot account for seasonal and age-related variation and cannot be used to measure differences in brain structure.
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Vocal learners such as humans and songbirds can learn to produce elaborate patterns of structurally organized vocalizations, whereas many other vertebrates such as non-human primates and most other bird groups either cannot or do so to a very limited degree. To explain the similarities among humans and vocal-learning birds and the differences with other species, various theories have been proposed. One set of theories are motor theories, which underscore the role of the motor system as an evolutionary substrate for vocal production learning. For instance, the motor theory of speech and song perception proposes enhanced auditory perceptual learning of speech in humans and song in birds, which suggests a considerable level of neurobiological specialization. Another, a motor theory of vocal learning origin, proposes that the brain pathways that control the learning and production of song and speech were derived from adjacent motor brain pathways. Another set of theories are cognitive theories, which address the interface between cognition and the auditory-vocal domains to support language learning in humans. Here we critically review the behavioral and neurobiological evidence for parallels and differences between the so-called vocal learners and vocal non-learners in the context of motor and cognitive theories. In doing so, we note that behaviorally vocal-production learning abilities are more distributed than categorical, as are the auditory-learning abilities of animals. We propose testable hypotheses on the extent of the specializations and cross-species correspondences suggested by motor and cognitive theories. We believe that determining how spoken language evolved is likely to become clearer with concerted efforts in testing comparative data from many non-human animal species.
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Biologists have long been fascinated by the exceptionally high diversity displayed by some evolutionary groups. Adaptive radiation in such clades is not only spectacular, but is also an extremely complex process influenced by a variety of ecological, genetic, and developmental factors and strongly dependent on historical contingencies. Using modeling approaches, we identify 10 general patterns concerning the temporal, spatial, and genetic/morphological properties of adaptive radiation. Some of these are strongly supported by empirical work, whereas for others, empirical support is more tentative. In almost all cases, more data are needed. Future progress in our understanding of adaptive radiation will be most successful if theoretical and empirical approaches are integrated, as has happened in other areas of evolutionary biology.
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Inter- and intraspecific variations in the sizes of specific avian brain regions correspond to the complexity of the behaviour that they govern. However, no study has demonstrated a relationship between gross brain size and behavioural complexity, a hypothesis that has been proposed to explain the unusually large human brain. I show, using X-rays of museum specimens, that species of bowerbirds that build bowers have relatively larger brains than both related and ecologically similar but unrelated species that do not build bowers. Bower design varies across species from simple cleared courts to ornate, hut-like structures large enough to contain a small child. Furthermore, species building more complex bowers have relatively larger brains, both within each of the two different bower-building clades and across the family as a whole, controlling for phylogeny. Such gross differences in brain size are surprising and may reflect the range of cognitive processes necessary for successful bower building, The relationships are strongest for males, the bower-building sex, although there is a similar trend in females. Because the size and complexity of bower design is targeted by female choice, the observation that relative brain size is related to bower complexity suggests that sexual selection may drive gross brain enlargement.
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Evidence is accumulating that species traits can spur their evolutionary diversification by influencing niche shifts, range expansions, and extinction risk. Previous work has shown that larger brains (relative to body size) facilitate niche shifts and range expansions by enhancing behavioral plasticity but whether larger brains also promote evolutionary diversification is currently backed by insufficient evidence. We addressed this gap by combining a brain size dataset for >1900 avian species worldwide with estimates of diversification rates based on two conceptually different phylogenetic‐based approaches. We found consistent evidence that lineages with larger brains (relative to body size) have diversified faster than lineages with relatively smaller brains. The best supported trait‐dependent model suggests that brain size primarily affects diversification rates by increasing speciation rather than decreasing extinction rates. In addition, we found that the effect of relatively brain size on species‐level diversification rate is additive to the effect of other intrinsic and extrinsic factors. Altogether, our results highlight the importance of brain size as an important factor in evolution and reinforce the view that intrinsic features of species have the potential to influence the pace of evolution.
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The fossil record and recent molecular phylogenies support an extraordinary early-Cenozoic radiation of crown birds (Neornithes) after the Cretaceous-Paleogene (K-Pg) mass extinction [1-3]. However, questions remain regarding the mechanisms underlying the survival of the deepest lineages within crown birds across the K-Pg boundary, particularly since this global catastrophe eliminated even the closest stem-group relatives of Neornithes [4]. Here, ancestral state reconstructions of neornithine ecology reveal a strong bias toward taxa exhibiting predominantly non-arboreal lifestyles across the K-Pg, with multiple convergent transitions toward predominantly arboreal ecologies later in the Paleocene and Eocene. By contrast, ecomorphological inferences indicate predominantly arboreal lifestyles among enantiornithines, the most diverse and widespread Mesozoic avialans [5-7]. Global paleobotanical and palynological data show that the K-Pg Chicxulub impact triggered widespread destruction of forests [8, 9]. We suggest that ecological filtering due to the temporary loss of significant plant cover across the K-Pg boundary selected against any flying dinosaurs (Avialae [10]) committed to arboreal ecologies, resulting in a predominantly non-arboreal post-extinction neornithine avifauna composed of total-clade Palaeognathae, Galloanserae, and terrestrial total-clade Neoaves that rapidly diversified into the broad range of avian ecologies familiar today. The explanation proposed here provides a unifying hypothesis for the K-Pg-associated mass extinction of arboreal stem birds, as well as for the post-K-Pg radiation of arboreal crown birds. It also provides a baseline hypothesis to be further refined pending the discovery of additional neornithine fossils from the Latest Cretaceous and earliest Paleogene.
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Although reconstruction of the phylogeny of living birds has progressed tremendously in the last decade, the evolutionary history of Neoaves—a clade that encompasses nearly all living bird species—remains the greatest unresolved challenge in dinosaur systematics. Here we investigate avian phylogeny with an unprecedented scale of data: >390,000 bases of genomic sequence data from each of 198 species of living birds, representing all major avian lineages, and two crocodilian outgroups. Sequence data were collected using anchored hybrid enrichment, yielding 259 nuclear loci with an average length of 1,523 bases for a total data set of over 7.8 × 10⁷ bases. Bayesian and maximum likelihood analyses yielded highly supported and nearly identical phylogenetic trees for all major avian lineages. Five major clades form successive sister groups to the rest of Neoaves: (1) a clade including nightjars, other caprimulgiforms, swifts, and hummingbirds; (2) a clade uniting cuckoos, bustards, and turacos with pigeons, mesites, and sandgrouse; (3) cranes and their relatives; (4) a comprehensive waterbird clade, including all diving, wading, and shorebirds; and (5) a comprehensive landbird clade with the enigmatic hoatzin (Opisthocomus hoazin) as the sister group to the rest. Neither of the two main, recently proposed Neoavian clades—Columbea and Passerea—were supported as monophyletic. The results of our divergence time analyses are congruent with the palaeontological record, supporting a major radiation of crown birds in the wake of the Cretaceous–Palaeogene (K–Pg) mass extinction.
Article
Encephalization is a core concept in comparative neurobiology, aiming to quantify the neurological capacity of organisms. For measuring encephalization, many studies have employed relative brain sizes corrected for expected allometric scaling to body size. Here we highlight the utility of a multivariate geometric morphometric (GM) approach for visualizing and analyzing neuroanatomical shape variation associated with encephalization. GM readily allows the statistical evaluation of covariates, such as size, and many software tools exist for visualizing their effects on shape. Thus far, however, studies using GM have not attempted to translate the meaning of encephalization to shape data. As such, we tested the statistical relationship between size and encephalization quotients (EQs) to brain shape utilizing a broad interspecific sample of avian endocranial data. Although statistically significant, the analyses indicate that allometry accounts for <10% of total neuroanatomical shape variation. Notably, we find that EQs, despite being corrected for allometric scaling based on size, contain size-related neuroanatomical shape changes. In addition, much of what is traditionally considered encephalization comprises clade-specific trends in relative forebrain expansion, particularly driven by landbirds. EQs, therefore, fail to capture 90% of the total neuroanatomical variation after correcting for allometry and shared phylogenetic history. Moving forward, GM techniques provide crucial tools for investigating key drivers of this vast, largely unexplored aspect of avian brain morphology.
Article
To understand the nature of the evolutionary process, it is of paramount importance that temporal patterns of change in biological traits are accurately documented. The paleontological record is, however, inherently incomplete, leaving researchers with only a limited set of observed taxonomic units (OTUs) to estimate broader patterns of biological change. In this context, phylogenetic comparative methods have been developed aiming to estimate patterns of phenotypic change through time based on a phylogenetic tree and a limited set of OTUs. Such methods typically employ mathematical models proposing how change is likely to have unfolded over time. The most commonly used model, Brownian motion (BM), assumes that average trait change is proportional to the square root of time and that the rate of evolution is stochastically constant across all branches. This, however, lies in contrast to the commonly agreed notion that many biological traits change at different rates along different branches of the tree of life. We present a method for inferring ancestral states that allows for different evolutionary rates along different branches of the phylogenetic tree. The goal is to include the effects of variation in rates of phenotypic change across phylogenetic space. Based on the available phenotypic and phylogenetic information, we estimate measures of the rate of evolution on each individual branch and, subsequently, these estimates are used to parameterize a multiple variance BM model inferring the phenotypic values at all internal nodes. We demonstrate the validity of our approach with a series of simulations and an empirical example. We show that values for internal nodes inferred using our approach are equivalent to those inferred with a constant variance BM model if phenotypic evolution occurs according to standard BM. When evolution occurs at different rates along different branches of the phylogeny, our approach greatly outperforms constant variance BM. We further demonstrate that our approach accurately detects bursts of change in phylogenetic space. An empirical analysis of the evolution of primate brain and body mass reveals that our approach yields an improved statistical fit relative to both traditional and recent methods, and provides estimates of nodal values that lie within a range expected based on the fossil record.
Article
The scaling of body parts is central to the expression of morphology across body sizes and to the generation of morphological diversity within and among species. Although patterns of scaling-relationship evolution have been well documented for over one hundred years, little is known regarding how selection acts to generate these patterns. In part, this is because it is unclear the extent to which the elements of log-linear scaling relationships - the intercept or mean trait size and the slope - can evolve independently. Here, using the wing-body size scaling relationship in Drosophila melanogaster as an empirical model, we use artificial selection to demonstrate that the slope of a morphological scaling relationship between an organ (the wing) and body size can evolve independently of mean organ or body size. We discuss our findings in the context of how selection likely operates on morphological scaling relationships in nature, the developmental basis for evolved changes in scaling, and the general approach of using individual-based selection experiments to study the expression and evolution of morphological scaling. This article is protected by copyright. All rights reserved.
Article
The detection of evolutionary shifts in trait evolution from extant taxa is motivated by the study of convergent evolution, or to correlate shifts in traits with habitat changes or with changes in other phenotypes. We propose here a phylogenetic lasso method to study trait evolution from comparative data and detect past changes in the expected mean trait values. We use the Ornstein-Uhlenbeck process, which can model a changing adaptive landscape over time and over lineages. Our method is very fast, running in minutes for hundreds of species, and can handle multiple traits. We also propose a phylogenetic Bayesian information criterion (pBIC) that accounts for the phylogenetic correlation between species, as well as for the complexity of estimating an unknown number of shifts at unknown locations in the phylogeny. This criterion does not suffer model overfitting and has high precision, so it offers a conservative alternative to other information criteria. Our re-analysis of Anolis lizard data suggests a more conservative scenario of morphological adaptation and convergence than previously proposed. Software is available on GitHub. This article is protected by copyright. All rights reserved.
Article
1.For the study of macroevolution, phenotypic data are analyzed across species on a dated phylogeny using phylogenetic comparative methods. In this context, the Ornstein-Uhlenbeck (OU) process is now being used extensively to model selectively-driven trait evolution, whereby a trait is attracted to a selection optimum μ.2.We report here theoretical properties of the maximum likelihood (ML) estimators for these parameters, including their non-uniqueness and inaccuracy, and show that theoretical expectations indeed apply to real trees. We provide necessary conditions for ML estimators to be well-defined and practical implications for model parametrization.3.We then show how these limitations carry over to difficulties in detecting shifts in selection regimes along a phylogeny. When the phylogenetic placement of these shifts is unknown, we identify a “large p - small n” problem where traditional model selection criteria fail and favor overly complex scenarios. Instead, we propose a modified criterion that is better adapted to change-point models.4.The challenges we identify here are inherent to trait evolution models on phylogenetic trees when observations are limited to present-day taxa, and require the addition of fossil taxa to be alleviated. We conclude with recommendations for empiricists.This article is protected by copyright. All rights reserved.
Article
Morphological allometry refers to patterns of covariance between body parts resulting from variation in body size. Whether measured during growth (ontogenetic allometry), among individuals at similar developmental stage (static allometry), or among populations or species (evolutionary allometry), allometric relationships are often tight and relatively invariant. Consequently, it has been suggested that allometries have low evolvability and could constrain phenotypic evolution by forcing evolving species along fixed trajectories. Alternatively, allometric relationships may result from natural selection for functional optimization. Despite nearly a century of active research, distinguishing between these alternatives remains difficult, partly due to wide differences in the meaning assigned to the term allometry. In particular, a broad use of the term, encompassing any monotonic relationship between body parts, has become common. This usage breaks the connection to the proportional growth regulation that motivated Huxley's original narrow-sense use of allometry to refer to power-law relationships between traits. Focusing on the narrow-sense definition of allometry, we review here evidence for and against the allometry-as-a-constraint hypothesis. Although the low evolvability and the evolutionary invariance of the static allometric slope observed in some studies suggest a possible constraining effect of this parameter on phenotypic evolution, the lack of knowledge about selection on allometry prevents firm conclusions.
Article
1. We present a method, 'SURFACE', that uses the Ornstein-Uhlenbeck stabilizing selection model to identify cases of convergent evolution using only continuous phenotypic characters and a phylogenetic tree. 2. SURFACE uses stepwise Akaike Information Criterion first to locate regime shifts on a tree, then to identify whether shifts are towards convergent regimes. Simulations can be used to test the hypothesis that a clade con-tains more convergence than expected by chance. 3. We demonstrate the method with an application to Hawaiian Tetragnatha spiders, and present numerical sim-ulations showing that the method has desirable statistical properties given data for multiple traits. 4. The R package surface is available as open source software from the Comprehensive R Archive Network.
Article
There is wide variation in brain shape among birds. Differences in brain dimensions reflect species-specific sensory capacities and behavioral repertoires that are shaped by environmental and biological factors during evolution. Most previous studies aimed at defining factors impacting brain shape have used volumetric or linear measurements. However, few have explored the quantitative indices of three-dimensional (3D) brain geometry that are absolutely imperative to understanding avian evolutionary history. This study aimed: (i) to explore the relationship between brain shape and overall brain size; and (ii) to assess the relationship between brain shape and orbital shape. Avian brain endocasts were reconstructed from computed tomography images and analyzed using 3D geometric morphometrics. Principal component analysis revealed dominant regional variations in avian brain shape and shape correlations between the telencephalon and cerebellum, between the cerebellum and myelencephalon, and between the diencephalon and optic tectum. Brain shape changes relative to total brain size were determined by multivariate regression analysis. Larger brain size was associated with a relatively slender telencephalon and differences in brain orientation. The correlation between brain shape and orbital shape was assessed by two-block partial least-squares analysis. Relatively round brains with a ventrally flexed brain base were associated with rounder orbits, while narrower brains with a flat brain base were associated with more elongated orbits. The shapes of functionally associated avian brain regions are correlated, and orbital size and shape are dominant factors influencing the overall shape of the avian brain.
Article
See what's new in the Second Edition: · Number of species included is increased from 6300 to over 8700, about 85% of the world's birds · Better data for many of the species included in the first edition - an exhaustive compilation of new data published from 1992 through 2007 · More comprehensive coverage of Latin America, Japan, Taiwan, Southeast Asia, and more coverage of research published in non-English language journals In 1992 the CRC Handbook of Avian Body Masses broke new ground by providing a compilation of body masses for 6300 species, about two-thirds of the world's species. The handbook instantly became the gold standard, cited in hundreds of scientific studies and a prominent fixture on the shelves of many ornithologists. Keeping the format that made the first edition so popular, the second edition features dramatic changes both in species coverage and the data quality. The new edition compiles the results of new samples that have been published for many of the birds included in the first edition, and data found for about 2400 new species, increasing the coverage to over 8700 species, about 85% of the world's birds. The order of species and families has been revised in the text to fit with the latest publications in avian taxonomy and systematics. The second edition includes an accompanying CD-ROM with a searchable electronic database.
Article
Comparative biologists often attempt to draw inferences about tempo and mode in evolution by comparing the fit of evolutionary models to phylogenetic comparative data consisting of a molecular phylogeny with branch lengths and trait measurements from extant taxa. These kinds of approaches ignore historical evidence for evolutionary pattern and process contained in the fossil record. In this article, we show through simulation that incorporation of fossil information dramatically improves our ability to distinguish among models of quantitative trait evolution using comparative data. We further suggest a novel Bayesian approach that allows fossil information to be integrated even when explicit phylogenetic hypotheses are lacking for extinct representatives of extant clades. By applying this approach to a comparative dataset comprising body sizes for caniform carnivorans, we show that incorporation of fossil information not only improves ancestral state estimates relative to those derived from extant taxa alone, but also results in preference of a model of evolution with trend toward large body size over alternative models such as Brownian motion or Ornstein-Uhlenbeck processes. Our approach highlights the importance of considering fossil information when making macroevolutionary inference, and provides a way to integrate the kind of sparse fossil information that is available to most evolutionary biologists.
Article
Tools are traditionally defined as objects that are used as an extension of the body and held directly in the hand or mouth. By these standards, a vulture breaking an egg by hitting it with a stone uses a tool, but a gull dropping an egg on a rock does not. This distinction between true and borderline (or proto-tool) cases has been criticized for its arbitrariness and anthropocentrism. We show here that relative size of the neostriatum and whole brain distinguish the true and borderline categories in birds using tools to obtain food or water. From two sources, the specialized literature on tools and an innovation data base gathered in the short note sections of 68 journals in 7 areas of the world, we collected 39 true (e.g. use of probes, hammers, sponges, scoops) and 86 borderline (e.g. bait fishing, battering and dropping on anvils, holding with wedges and skewers) cases of tool use in 104 species from 15 parvorders. True tool users have a larger mean residual brain size (regressed against body weight) than do users of borderline tools, confirming the distinction in the literature. In multiple regressions, residual brain size and residual size of the neostriatum (one of the areas in the avian telencephalon thought to be equivalent to the mammalian neocortex) are the best predictors of true tool use reports per taxon. Innovation rate is the best predictor of borderline tool use distribution. Despite the strong concentration of true tool use cases in Corvida and Passerida, independent constrasts suggest that common ancestry is not responsible for the association between tool use and size of the neostriatum and whole brain. Our results demonstrate that birds are more frequent tool users than usually thought and that the complex cognitive processes involved in tool use may have repeatedly co-evolved with large brains in several orders of birds.
Article
The hypothesis that large brains allow animals to produce novel behaviour patterns is supported by the correlation between brain size, corrected for body size, and the frequency of foraging innovations reported in the literature for both birds and primates. In birds, foraging innovations have been observed in over 800 species, and include behaviours that range from eating a novel food to using tools. Previous comparative studies have quantified innovativeness by summing all reports of innovative behaviour, regardless of the nature of the innovation. Here, we use the variety of foraging innovations recorded for birds to see which of two classic hypotheses best accounts for the relationship between innovativeness and brain size: the technical intelligence hypothesis or the opportunistic-generalism intelligence hypothesis. We classified 2182 innovation cases into 12 categories to quantify the diversity of innovations performed by each of 76 avian families. We found that families with larger brains had a greater repertoire of innovations, and that innovation diversity was a stronger predictor of residual brain size than was total number of innovations. Furthermore, the diversity of technical innovations displayed by bird families was a much better predictor of residual brain size than was the number of food type innovations, providing support for the technical intelligence hypothesis. Our results suggest that the cognitive capacity required to perform a wide variety of novel foraging techniques underpins the positive relationship between innovativeness and brain size in birds. We include a summary of innovation data for 803 species as Supplementary Material.
Article
In haplorhine primates, when the effect of body weight is removed, brain weight is correlated with maximum recorded life-span. In this paper we have analyzed the relationships between volumes of specific brain structures and life-span. When the effect of body weight is removed, the volumes of many brain structures are significantly, positively correlated with maximum recorded life-span. However, the volumes of the medulla and most first-order sensory structures do not correlate with life-span. The cerebellum is the brain structure that best correlates with life-span. Parts of the cerebellum are particularly vulnerable to age-related loss of mass in humans. For another measure of the life cycle, female reproductive age, a similar set of brain structures is significantly, positively correlated (again with the exceptions of the medulla and most first-order sensory structures). There are some differences between the structures correlated for life-span and female reproductive age. For example, the hippocampus and lateral geniculate nucleus correlate with female reproductive age but do not correlate with life-span. In strepsirhine primates, when the effect of body weight is removed, total brain weight does not significantly correlate with either life-span or female reproductive age. However, the volumes of some brain structures in strepsirhines do correlate with these life-cycle parameters. The centromedial complex of the amygdala is the only structure to correlate with life-span in both strepsirhine and haplorhine primates. This structure participates in the regulation of blood pressure and in the stress response, which may be key factors governing life-span.