The multiple contexts of brain scaling: Phenotypic integration in brain and behavioral evolution

Understanding the adaptive functions of increasing brain size have occupied scientists for decades. Here, taking the general perspective of the Extended Evolutionary Synthesis, the question of how brains change in size will be considered in two developmental frameworks. The first framework will consider the particular developmental mechanisms that control and generate brain mass, concentrating on neurogenesis in a comparative vertebrate context. The consequences of limited adult neurogenesis in mammals, and the dominating role of duration of neurogenesis for mammalian evolution will be discussed for the particular case of the teleost versus mammalian retina, and for paths of brain evolution more generally. The second framework examines brain mass in terms of life history, particularly the features of life history that correlate highly, if imperfectly, with brain mass, including duration of development to adolescence, duration of parental care, body and range size, and longevity. This covariation will be examined in light of current work on genetic causes and consequences of covariation in craniofacial bone groupings. The eventual development of a multivariate structure for understanding brain evolution which specifically integrates formerly separate layers of analysis is the ultimate goal.

Is there a prechordal region and an acroterminal domain in amphioxus?

This essay re-examines the singular case of the supposedly unique rostrally elongated notochord described classically in amphioxus. We start from our previous observations in hpf 21 larvae [Albuixech-Crespo et al., 2017] indicating that the brain vesicle has rostrally a rather standard hypothalamic molecular configuration. This correlates with the notochord across a possible rostromedian acroterminal hypothalamic domain . The notochord shows some molecular differences that specifically characterize its pre-acroterminal extension beyond its normal rostral end under the mamillary region. We explored an alternative interpretation that the putative extension of this notochord actually represents a variant form of the prechordal plate in amphioxus, some of whose cells would adopt the notochordal typology, but would lack notochordal patterning properties, and might have some (but not all) prechordal ones instead. We survey in detail the classic and recent literature on gastrulation, prechordal plate and notochord formation in amphioxus, compared the observed patterns with those of some other vertebrates of interest, and re-examine the literature on differential gene expression patterns in this rostralmost area of the head. We noted that previous literature failed at identifying the amphioxus prechordal primordia at appropriate stages. Under this interpretation, a consistent picture can be drawn for cephalochordates, tunicates, and vertebrates. Moreover, there is little evidence for an intrinsic capacity of the early notochord to grow rostralwards (it normally elongates caudalwards). Altogether, we conclude that the hypothesis of a prechordal nature of the elongated amphioxus notochord is consistent with the evidence presented.

Timing as a mechanism of development and evolution in the cerebral cortex

One of the biggest mysteries in neurobiology concerns the mechanisms responsible for the diversification of the brain over different time scales i.e. during development and evolution. Subtle differences in the timing of biological processes during development, e.g. onset, offset, duration, speed and sequence, can trigger large changes in phenotypic outcomes. At the level of a single organism, altered timing of developmental events can lead to individual variability, as well as malformation and disease. At the level of phylogeny, there are known interspecies differences in the timing of developmental events, and this is thought to be an important factor that drives phenotypic variation across evolution, known as heterochrony. A particularly striking example of phenotypic variation is the evolution of human cognitive abilities, which has largely been attributed to the development of the mammalian-specific neocortex and its subsequent expansion in higher primates. Here, I review how the timing of different aspects of cortical development specifies developmental outcomes within species, including processes of cell proliferation and differentiation, neuronal migration and lamination, and axonal targeting and circuit maturation. Some examples of the ways that different processes might “keep time” in the cortex are explored, reviewing potential cell-intrinsic and -extrinsic mechanisms. Further, by combining this knowledge with known differences in timing across species, timing changes that may have occurred during evolution are identified, which perhaps drove the phylogenetic diversification of neocortical structure and function.

Sickness and the social brain: How the immune system regulates behavior across species

Many instances of sickness critically involve the immune system. The immune system talks to the brain in a bi-directional loop. This discourse affords the immune system immense control, such that it can influence behavior and optimize recovery from illness. These behavioral responses to infection are called sickness behaviors and can manifest in many ways, including changes in mood, motivation, or energy. Fascinatingly, most of these changes are conserved across species, and most organisms demonstrate some form of sickness behaviors. One of the most interesting sickness behaviors, and not immediately obvious, is altered sociability. Here, we discuss how the immune system impacts social behavior, by examining the brain regions and immune mediators involved in this process. We first outline how social behavior changes in response to infection in various species. Next, we explore which brain regions control social behavior and their evolutionary origins. Finally, we describe which immune mediators establish the link between illness and social behavior, in the context of both normal development and infection. Overall, we hope to make clear the striking similarities between the mechanisms that facilitate changes in sociability in derived and ancestral vertebrate, as well as invertebrate, species.

Immunolabeling provides evidence for subregions in the songbird nucleus accumbens and suggests a context-dependent role in song in male European starlings (Sturnus vulgaris)

Birdsong is well known for its role in mate attraction during the breeding season. However, many birds, including European starlings (Sturnus vulgaris), also sing outside the breeding season as part of large flocks. Song in a breeding context can be extrinsically rewarded by mate attraction; however, song in non-breeding flocks, referred to here as gregarious song, results in no obvious extrinsic reward and is proposed to be intrinsically rewarded. The nucleus accumbens (NAc) is a brain region well-known to mediate reward and motivation, which suggests it is an ideal candidate to regulate reward associated with gregarious song. The goal of this study was to provide new histochemical information on the songbird NAc and its subregions (rostral pole, core, and shell), and to begin to determine subregion-specific contributions to gregarious song in male starlings. We examined immunolabeling for tyrosine hydroxylase (TH), neurotensin, and enkephalin (ENK) in NAc. We then examined the extent to which gregarious and sexually-motivated song differentially correlated with immunolabeling for the immediate early genes FOS and ZENK in each subdivision of NAc. We found that TH and ENK labeling within subregions of the starling NAc was generally similar to patterns seen in the core and shell of NAc in mammals and birds. Additionally, we found that gregarious song, but not sexually-motivated song, positively correlated with FOS in all NAc subregions. Our observations provide further evidence for distinct subregions within the songbird NAc and suggest the NAc may play an important role in regulating gregarious song in songbirds.

Evolutionary and allometric insights into anuran auditory sensitivity and morphology

As species change through evolutionary time, the neurological and morphological structures that underly behavioral systems typically remain coordinated. This is especially important for communication systems, in which these structures must remain coordinated both within and between senders and receivers for successful information transfer. The acoustic communication of anurans (“frogs”) offers an excellent system to ask when and how such coordination is maintained, and to allow researchers to dissociate allometric effects from independent correlated evolution. Anurans constitute one of the most speciose groups of vocalizing vertebrates and females typically rely on vocalizations to localize males for reproduction. Here, we compile and compare data on various aspects of auditory morphology, hearing sensitivity and call dominant frequency across 81 species of anurans. We find robust, phylogenetically independent scaling effects of body size for all features measured. Furthermore, after accounting for body size, we find preliminary evidence that morphological evolution beyond allometry can correlate with hearing sensitivity and dominant frequency. These data provide foundational results regarding constraints imposed by body size on communication systems and motivate further data collection and analysis using comparative approaches across the numerous anuran species.

Can the Dynamic Colouration and Patterning of Bluelined Goatfish (Mullidae; Upeneichthys lineatus) Be Perceived by Conspecifics?

Bluelined goatfish (<i>Upeneichthys lineatus</i>) exhibit dynamic body colour changes and transform rapidly from a pale, buff/white, horizontally banded pattern to a conspicuous, vertically striped, red pattern when foraging. This red pattern is potentially an important foraging signal for communication with conspecifics, provided that <i>U. lineatus</i> can detect and discriminate the pattern. Using both physiological and behavioural experiments, we first examined whether <i>U. lineatus</i> possess visual pigments with sensitivity to long (“red”) wavelengths of light, and whether they can discriminate the colour red. Microspectrophotometric measurements of retinal photoreceptors showed that while <i>U. lineatus</i>lack visual pigments dedicated to the red part of the spectrum, their pigments likely confer some sensitivity in this spectral band. Behavioural colour discrimination experiments suggested that <i>U. lineatus</i>can distinguish a red reward stimulus from a grey distractor stimulus of variable brightness. Furthermore, when presented with red stimuli of varying brightness they could mostly discriminate the darker and lighter reds from the grey distractor. We also obtained anatomical estimates of visual acuity, which suggest that <i>U. lineatus</i> can resolve the contrasting bands of conspecifics approximately 7 m away in clear waters. Finally, we measured the spectral reflectance of the red and white colouration on the goatfish body. Visual models suggest that <i>U. lineatus</i> can discriminate both chromatic and achromatic differences in body colouration where longer wavelength light is available. This study demonstrates that <i>U. lineatus</i> have the capacity for colour vision and can likely discriminate colours in the long-wavelength region of the spectrum where the red body pattern reflects light strongly. The ability to see red may therefore provide an advantage in recognising visual signals from conspecifics. This research furthers our understanding of how visual signals have co-evolved with visual abilities, and the role of visual communication in the marine environment.

Effects of Frequency on the Directional Auditory Sensitivity of Northern Saw-Whet Owls (Aegolius acadicus)

Many animals use sound as a medium for detecting or locating potential prey items or predation threats. Northern saw-whet owls (<i>Aegolius acadicus</i>) are particularly interesting in this regard, as they primarily rely on sound for hunting in darkness, but are also subject to predation pressure from larger raptors. We hypothesized that these opposing tasks should favor sensitivity to low-frequency sounds arriving from many locations (potential predators) and high-frequency sounds below the animal (ground-dwelling prey items). Furthermore, based on the morphology of the saw-whet owl skull and the head-related transfer functions of related species, we expected that the magnitude of changes in sensitivity across spatial locations would be greater for higher frequencies than low frequencies (i.e., more “directional” at high frequencies). We used auditory-evoked potentials to investigate the frequency-specific directional sensitivity of Northern saw-whet owls to acoustic signals. We found some support for our hypothesis, with smaller-magnitude changes in sensitivity across spatial locations at lower frequencies and larger-magnitude changes at higher frequencies. In general, owls were most sensitive to sounds originating in front of and above their heads, but at 8 kHz there was also an area of high sensitivity below the animals. Our results suggest that the directional hearing of saw-whet owls should allow for both predator and prey detection.

Anuran Vocal Communication: Effects of Genome Size, Cell Number and Cell Size

Significant variation in genome size occurs among anuran amphibians and can affect cell size and number. In the gray treefrog complex in North America increases in cell size in autotriploids of the diploid (Hyla chrysoscelis) altered the temporal structure of mate-attracting vocalizations and auditory selectivity for these properties. Here we show that the tetraploid species (Hyla versicolor) also has significantly fewer brain neurons than H. chrysoscelis. With regard to cell size in tissues involved in vocal communication, spinal motor neurons were larger in tetraploids than in diploids and comparable to differences in erythrocyte size; smaller increases were found in one of the three auditory centers in the torus semicircularis. Future studies should address questions about how environmental conditions during development affect cell numbers and size and the causal relationships between these cellular changes and the vocal communication system.

High Encephalization in a Fossil Rorqual Illuminates Baleen Whale Brain Evolution

Baleen whales are considered underencephalized mammals due to their reduced brain size with respect to their body size (encephalization quotient [EQ] &#x3c;&#x3c; 1). Despite their low EQ, mysticetes exhibit complex behavioral patterns in terms of motor abilities, vocal repertoire, and cultural learning. Very scarce information is available about the morphological evolution of the brain in this group; this makes it difficult to investigate the historical changes in brain shape and size in order to relate the origin of the complex mysticete behavioral repertoire to the evolution of specific neural substrates. Here, the first description of the virtual endocast of a fossil balaenopterid species, <i>Marzanoptera tersillae</i> from the Italian Pliocene, reveals an EQ of around 3, which is exceptional for baleen whales. The endocast showed a morphologically different organization of the brain in this fossil whale as the cerebral hemispheres are anteroposteriorly shortened, the cerebellum lacks the posteromedial expansion of the cerebellar hemispheres, and the cerebellar vermis is unusually reduced. The comparative reductions of the cerebral and cerebellar hemispheres suggest that the motor behavior of <i>M. tersillae</i> probably was less sophisticated than that exhibited by the extant rorqual and humpback species. The presence of an EQ value in this fossil species that is around 10 times higher than that of extant mysticetes opens new questions about brain evolution and provides new, invaluable information about the evolutionary path of morphological and size change in the brain of baleen whales.