Condition dependence, developmental plasticity, and cognition: implications for ecology and evolution.
ABSTRACT: Across taxa, both neural growth and cognitive function show considerable developmental plasticity. Data from studies of decision making, learning, and discrimination demonstrate that early life conditions have an impact on subsequent neural growth, maintenance, and cognition, with important ecological and evolutionary implications. Here, we provide a synthesis of the evidence that spatial and vocal learning are condition dependent, addressing what is known about their physiological control and the functional explanations. Neural investment is predicted to be affected by environmental conditions, but the shape of the response should depend on the fitness benefits of the cognitive traits under control. From an evolutionary perspective, traits promoting resistance to environmental perturbations should be favored when the cognitive trait is a crucial determinant of fitness.
Project description:In birds, vocal learning enables the production of sexually selected complex songs, dialects and song copy matching. But stressful conditions during development have been shown to affect song production and complexity, mediated by changes in neural development. However, to date, no studies have tested whether early-life stress affects the neural processes underlying vocal learning, in contrast to song production. Here, we hypothesized that developmental stress alters auditory memory formation and neural processing of song stimuli. We experimentally stressed male nestling zebra finches and, in two separate experiments, tested their neural responses to song playbacks as adults, using either immediate early gene (IEG) expression or electrophysiological response. Once adult, nutritionally stressed males exhibited a reduced response to tutor song playback, as demonstrated by reduced expressions of two IEGs (Arc and ZENK) and reduced neuronal response, in both the caudomedial nidopallium (NCM) and mesopallium (CMM). Furthermore, nutritionally stressed males also showed impaired neuronal memory for novel songs heard in adulthood. These findings demonstrate, for the first time, that developmental conditions affect auditory memories that subserve vocal learning. Although the fitness consequences of such memory impairments remain to be determined, this study highlights the lasting impact early-life experiences can have on cognitive abilities.
Project description:Natural selection can act on between-individual variation in cognitive abilities, yet evolutionary responses depend on the presence of underlying genetic variation. It is, therefore, crucial to determine the relative extent of genetic versus environmental control of these among-individual differences in cognitive traits to understand their causes and evolutionary potential. We investigated heritability of associative learning performance and of a cognitive judgement bias (optimism), as well as their covariation, in a captive pedigree-bred population of red junglefowl (Gallus gallus, n > 300 chicks over 5 years). We analysed performance in discriminative and reversal learning (two facets of associative learning), and cognitive judgement bias, by conducting animal models to disentangle genetic from environmental contributions. We demonstrate moderate heritability for reversal learning, and weak to no heritability for optimism and discriminative learning, respectively. The two facets of associative learning were weakly negatively correlated, consistent with hypothesized trade-offs underpinning individual cognitive styles. Reversal, but not discriminative learning performance, was associated with judgement bias; less optimistic individuals reversed a previously learnt association faster. Together these results indicate that genetic and environmental contributions differ among traits. While modular models of cognitive abilities predict a lack of common genetic control for different cognitive traits, further investigation is required to fully ascertain the degree of covariation between a broader range of cognitive traits and the extent of any shared genetic control.This article is part of the theme issue 'Causes and consequences of individual differences in cognitive abilities'.
Project description:Contact zones between subspecies or closely related species offer valuable insights into speciation processes. A typical feature of such zones is the presence of clinal variation in multiple traits. The nature of these traits and the concordance among clines are expected to influence whether and how quickly speciation will proceed. Learned signals, such as vocalizations in species having vocal learning (e.g. humans, many birds, bats and cetaceans), can exhibit rapid change and may accelerate reproductive isolation between populations. Therefore, particularly strong concordance among clines in learned signals and population genetic structure may be expected, even among continuous populations in the early stages of speciation. However, empirical evidence for this pattern is often limited because differences in vocalisations between populations are driven by habitat differences or have evolved in allopatry. We tested for this pattern in a unique system where we may be able to separate effects of habitat and evolutionary history. We studied geographic variation in the vocalizations of the crimson rosella (Platycercus elegans) parrot species complex. Parrots are well known for their life-long vocal learning and cognitive abilities. We analysed contact calls across a ca 1300 km transect encompassing populations that differed in neutral genetic markers and plumage colour. We found steep clinal changes in two acoustic variables (fundamental frequency and peak frequency position). The positions of the two clines in vocal traits were concordant with a steep cline in microsatellite-based genetic variation, but were discordant with the steep clines in mtDNA, plumage and habitat. Our study provides new evidence that vocal variation, in a species with vocal learning, can coincide with areas of restricted gene flow across geographically continuous populations. Our results suggest that traits that evolve culturally can be strongly associated with reduced gene flow between populations, and therefore may promote speciation, even in the absence of other barriers.
Project description:<h4>Background</h4>Floral nectar is an important determinant of plant-pollinator interactions and an integral component of pollination syndromes, suggesting it is under pollinator-mediated selection. However, compared to floral display traits, we know little about the evolutionary ecology of nectar. Combining a literature review with a meta-analysis approach, we summarize the evidence for heritable variation in nectar traits and link this variation to pollinator response and plant fitness. We further review associations between nectar traits and floral signals and discuss them in the context of honest signalling and targets of selection.<h4>Scope</h4>Although nectar is strongly influenced by environmental factors, heritable variation in nectar production rate has been documented in several populations (mean h2 = 0.31). Almost nothing is known about heritability of other nectar traits, such as sugar and amino acid concentrations. Only a handful of studies have quantified selection on nectar traits, and few find statistically significant selection. Pollinator responses to nectar traits indicate they may drive selection, but studies tying pollinator preferences to plant fitness are lacking. So far, only one study conclusively identified pollinators as selective agents on a nectar trait, and the role of microbes, herbivores, nectar robbers and abiotic factors in nectar evolution is largely hypothetical. Finally, there is a trend for positive correlations among floral cues and nectar traits, indicating honest signalling of rewards.<h4>Conclusions</h4>Important progress can be made by studies that quantify current selection on nectar in natural populations, as well as experimental approaches that identify the target traits and selective agents involved. Signal-reward associations suggest that correlational selection may shape evolution of nectar traits, and studies exploring these more complex forms of natural selection are needed. Many questions about nectar evolution remain unanswered, making this a field ripe for future research.
Project description:Mouse ultrasonic vocalizations (USVs) are often used as behavioral readouts of internal states, to measure effects of social and pharmacological manipulations, and for behavioral phenotyping of mouse models for neuropsychiatric and neurodegenerative disorders. However, little is known about the neurobiological mechanisms of rodent USV production. Here we discuss the available data to assess whether male mouse song behavior and the supporting brain circuits resemble those of known vocal non-learning or vocal learning species. Recent neurobiology studies have demonstrated that the mouse USV brain system includes motor cortex and striatal regions, and that the vocal motor cortex sends a direct sparse projection to the brainstem vocal motor nucleus ambiguous, a projection previously thought be unique to humans among mammals. Recent behavioral studies have reported opposing conclusions on mouse vocal plasticity, including vocal ontogeny changes in USVs over early development that might not be explained by innate maturation processes, evidence for and against a role for auditory feedback in developing and maintaining normal mouse USVs, and evidence for and against limited vocal imitation of song pitch. To reconcile these findings, we suggest that the trait of vocal learning may not be dichotomous but encompass a broad spectrum of behavioral and neural traits we call the continuum hypothesis, and that mice possess some of the traits associated with a capacity for limited vocal learning.
Project description:Like human speech, birdsong is a complex vocal behavior that is acquired by sensorimotor learning based on coordination of auditory input and vocal output to mimic memorized tutor song. Here we investigate neural circuits for vocal learning and production in deafened songbirds to elucidate how sensory-input regulate genetic and epigenetic property of vocal development and its associated gene expression dynamics. Compared with audition-intact birds, in deafened zebra finches, the vocal development is delayed but song crystallization is observed at more than three times later, producing individually different but structured vocal patterns. In contrast to the distinct difference of vocal ontogeny between audition (+) and (-), unexpectedly, developmental regulation of gene expression dynamics is strictly conserved with age-locked trend in vocal motor circuit in both intact and deafened birds, indicating sensory-input independent robustness of developmental gene expression dynamics in the motor circuit for sensorimotor learning. This discrepancy between outward vocal phenotype and inward gene expression dynamics provides new insight into neural regulation at closing of the critical period for vocal learning by two different forms: auditory inputs-dependent ‘active’ crystallization and gene expression dynamics-mediated ‘passive’ crystallization. We collected brain samples from intact and early-deafened birds (deafened at day-post hatch 17-23) under silent and dark condition. Song nuclei in vocal motor circuit, HVC and RA tissue samples (juvenile; n = 3, young; n = 3, old; n = 3 of intact and early-deafened birds for HVC and RA) were laser-microdissected from total 24 birds (intact; n = 12, early-deafened; n = 12). Each sample was hybridized to a single array, totaling 36 arrays. Birds were selected per slide such that early-deafened birds were paired with intact birds. To minimize possible interslide bias or batch effects, intact and early-deafened bird samples matching with brain area and age conditions were hybridized side by side on same array glass.
Project description:Mechanisms for the evolution of convergent behavioral traits are largely unknown. Vocal learning is one such trait that evolved multiple times and is necessary in humans for the acquisition of spoken language. Among birds, vocal learning is evolved in songbirds, parrots, and hummingbirds. Each time similar forebrain song nuclei specialized for vocal learning and production have evolved. This finding led to the hypothesis that the behavioral and neuroanatomical convergences for vocal learning could be associated with molecular convergence. We previously found that the neural activity-induced gene dual specificity phosphatase 1 (dusp1) was up-regulated in non-vocal circuits, specifically in sensory-input neurons of the thalamus and telencephalon; however, dusp1 was not up-regulated in higher order sensory neurons or motor circuits. Here we show that song motor nuclei are an exception to this pattern. The song nuclei of species from all known vocal learning avian lineages showed motor-driven up-regulation of dusp1 expression induced by singing. There was no detectable motor-driven dusp1 expression throughout the rest of the forebrain after non-vocal motor performance. This pattern contrasts with expression of the commonly studied activity-induced gene egr1, which shows motor-driven expression in song nuclei induced by singing, but also motor-driven expression in adjacent brain regions after non-vocal motor behaviors. In the vocal non-learning avian species, we found no detectable vocalizing-driven dusp1 expression in the forebrain. These findings suggest that independent evolutions of neural systems for vocal learning were accompanied by selection for specialized motor-driven expression of the dusp1 gene in those circuits. This specialized expression of dusp1 could potentially lead to differential regulation of dusp1-modulated molecular cascades in vocal learning circuits.
Project description:Humans and songbirds share the key trait of vocal learning, manifested in speech and song, respectively. Striking analogies between these behaviours include that both are acquired during developmental critical periods when the brain's ability for vocal learning peaks. Both behaviours show similarities in the overall architecture of their underlying brain areas, characterized by cortico-striato-thalamic loops and direct projections from cortical neurons onto brainstem motor neurons that control the vocal organs. These neural analogies extend to the molecular level, with certain song control regions sharing convergent transcriptional profiles with speech-related regions in the human brain. This evolutionary convergence offers an unprecedented opportunity to decipher the shared neurogenetic underpinnings of vocal learning. A key strength of the songbird model is that it allows for the delineation of activity-dependent transcriptional changes in the brain that are driven by learned vocal behaviour. To capitalize on this advantage, we used previously published datasets from our laboratory that correlate gene co-expression networks to features of learned vocalization within and after critical period closure to probe the functional relevance of genes implicated in language. We interrogate specific genes and cellular processes through converging lines of evidence: human-specific evolutionary changes, intelligence-related phenotypes and relevance to vocal learning gene co-expression in songbirds. This article is part of the theme issue 'What can animal communication teach us about human language?'
Project description:Complex learned behavior is influenced throughout development by both genetic and environmental factors. Birdsong, like human speech, is a complex vocal behavior acquired through sensorimotor learning and is based on coordinated auditory input and vocal output to mimic tutor song. Song is primarily learned during a specific developmental stage called the critical period. Although auditory input is crucial for acquiring complex vocal patterns, its exact role in neural circuit maturation for vocal learning and production is not well understood. Using audition-deprived songbirds, we examined whether auditory experience affects developmental gene expression in the major elements of neural circuits that mediate vocal learning and production. Compared with intact zebra finches, early-deafened zebra finches showed excessively delayed vocal development, but their songs eventually crystallized. In contrast to the different rates of song development between the intact and deafened birds, developmental gene expression in the motor circuit is conserved in an age-dependent manner from the juvenile stage until the older adult stage, even in the deafened birds, which indicates the audition-independent robustness of gene expression dynamics during development. Furthermore, even after adult deafening, which degrades crystallized song, the deteriorated songs ultimately restabilized at the same point when the early-deafened birds stabilized their songs. These results indicate a genetic program-associated inevitable termination of vocal plasticity that results in audition-independent vocal crystallization.
Project description:Vocal learning, in which animals modify their vocalizations based on social experience, has evolved in several lineages of mammals and birds, including humans. Despite much attention, the question of how this key cognitive trait has evolved remains unanswered. The motor theory for the origin of vocal learning posits that neural centres specialized for vocal learning arose from adjacent areas in the brain devoted to general motor learning. One prediction of this hypothesis is that visual displays that rely on complex motor patterns may also be learned in taxa with vocal learning. While learning of both spoken and gestural languages is well documented in humans, the occurrence of learned visual displays has rarely been examined in non-human animals. We tested for geographical variation consistent with learning of visual displays in long-billed hermits ( Phaethornis longirostris), a lek-mating hummingbird that, like humans, has both learned vocalizations and elaborate visual displays. We found lek-level signatures in both vocal parameters and visual display features, including display element proportions, sequence syntax and fine-scale parameters of elements. This variation was not associated with genetic differentiation between leks. In the absence of genetic differences, geographical variation in vocal signals at small scales is most parsimoniously attributed to learning, suggesting a significant role of social learning in visual display ontogeny. The co-occurrence of learning in vocal and visual displays would be consistent with a parallel evolution of these two signal modalities in this species.