Persistent vocal learning in an aging open-ended learner reflected in neural FoxP2 expression.

BACKGROUND: Most vocal learning species exhibit an early critical period during which their vocal control neural circuitry facilitates the acquisition of new vocalizations. Some taxa, most notably humans and parrots, retain some degree of neurobehavioral plasticity throughout adulthood, but both the extent of this plasticity and the neurogenetic mechanisms underlying it remain unclear. Differential expression of the transcription factor FoxP2 in both songbird and parrot vocal control nuclei has been identified previously as a key pattern facilitating vocal learning. We hypothesize that the resilience of vocal learning to cognitive decline in open-ended learners will be reflected in an absence of age-related changes in neural FoxP2 expression. We tested this hypothesis in the budgerigar (Melopsittacus undulatus), a small gregarious parrot in which adults converge on shared call types in response to shifts in group membership. We formed novel flocks of 4 previously unfamiliar males belonging to the same age class, either "young adult" (6 mo - 1 year) or "older adult" (≥ 3 year), and then collected audio-recordings over a 20-day learning period to assess vocal learning ability. Following behavioral recording, immunohistochemistry was performed on collected neural tissue to measure FoxP2 protein expression in a parrot vocal learning center, the magnocellular nucleus of the medial striatum (MMSt), and its adjacent striatum. RESULTS: Although older adults show lower vocal diversity (i.e. repertoire size) and higher absolute levels of FoxP2 in the MMSt than young adults, we find similarly persistent downregulation of FoxP2 and equivalent vocal plasticity and vocal convergence in the two age cohorts. No relationship between individual variation in vocal learning measures and FoxP2 expression was detected. CONCLUSIONS: We find neural evidence to support persistent vocal learning in the budgerigar, suggesting resilience to aging in the open-ended learning program of this species. The lack of a significant relationship between FoxP2 expression and individual variability in vocal learning performance suggests that other neurogenetic mechanisms could also regulate this complex behavior.

Individual identity information persists in learned calls of introduced parrot populations.

Animals can actively encode different types of identity information in learned communication signals, such as group membership or individual identity. The social environments in which animals interact may favor different types of information, but whether identity information conveyed in learned signals is robust or responsive to social disruption over short evolutionary timescales is not well understood. We inferred the type of identity information that was most salient in vocal signals by combining computational tools, including supervised machine learning, with a conceptual framework of "hierarchical mapping", or patterns of relative acoustic convergence across social scales. We used populations of a vocal learning species as a natural experiment to test whether the type of identity information emphasized in learned vocalizations changed in populations that experienced the social disruption of introduction into new parts of the world. We compared the social scales with the most salient identity information among native and introduced range monk parakeet (Myiopsitta monachus) calls recorded in Uruguay and the United States, respectively. We also evaluated whether the identity information emphasized in introduced range calls changed over time. To place our findings in an evolutionary context, we compared our results with another parrot species that exhibits well-established and distinctive regional vocal dialects that are consistent with signaling group identity. We found that both native and introduced range monk parakeet calls displayed the strongest convergence at the individual scale and minimal convergence within sites. We did not identify changes in the strength of acoustic convergence within sites over time in the introduced range calls. These results indicate that the individual identity information in learned vocalizations did not change over short evolutionary timescales in populations that experienced the social disruption of introduction. Our findings point to exciting new research directions about the robustness or responsiveness of communication systems over different evolutionary timescales.

Evidence for maintenance of key components of vocal learning in ageing budgerigars despite diminished affiliative social interaction.

In some species, the ability to acquire new vocalizations persists into adulthood and may be an important mediator of social interactions. While it is generally assumed that vocal learning persists undiminished throughout the lifespan of these open-ended learners, the stability of this trait remains largely unexplored. We hypothesize that vocal learning exhibits senescence, as is typical of complex cognitive traits, and that this decline relates to age-dependent changes in social behaviour. The budgerigar (Melopsittacus undulatus), an open-ended learner that develops new contact call types that are shared with social associates upon joining new flocks, provides a robust assay for measuring the effects of ageing on vocal learning ability. We formed captive flocks of 4 previously unfamiliar adult males of the same age class, either 'young adults' (6 mo-1 y) or 'older adults' (≥ 3 y), and concurrently tracked changes in contact call structure and social interactions over time. Older adults exhibited decreased vocal diversity, which may be related to sparser and weaker affiliative bonds observed in older adults. Older adults, however, displayed equivalent levels of vocal plasticity and vocal convergence compared to young adults, suggesting that many components of vocal learning are largely maintained into later adulthood in an open-ended learner.

Phylogenomic Analysis of the Parrots of the World Distinguishes Artifactual from Biological Sources of Gene Tree Discordance.

Gene tree discordance is expected in phylogenomic trees and biological processes are often invoked to explain it. However, heterogeneous levels of phylogenetic signal among individuals within data sets may cause artifactual sources of topological discordance. We examined how the information content in tips and subclades impacts topological discordance in the parrots (Order: Psittaciformes), a diverse and highly threatened clade of nearly 400 species. Using ultraconserved elements from 96% of the clade's species-level diversity, we estimated concatenated and species trees for 382 ingroup taxa. We found that discordance among tree topologies was most common at nodes dating between the late Miocene and Pliocene, and often at the taxonomic level of the genus. Accordingly, we used two metrics to characterize information content in tips and assess the degree to which conflict between trees was being driven by lower-quality samples. Most instances of topological conflict and nonmonophyletic genera in the species tree could be objectively identified using these metrics. For subclades still discordant after tip-based filtering, we used a machine learning approach to determine whether phylogenetic signal or noise was the more important predictor of metrics supporting the alternative topologies. We found that when signal favored one of the topologies, the noise was the most important variable in poorly performing models that favored the alternative topology. In sum, we show that artifactual sources of gene tree discordance, which are likely a common phenomenon in many data sets, can be distinguished from biological sources by quantifying the information content in each tip and modeling which factors support each topology. [Historical DNA; machine learning; museomics; Psittaciformes; species tree.].

Coevolution of relative brain size and life expectancy in parrots.

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 cognitivebuffer 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.

Understanding Organismal Capacity to Respond to Anthropogenic Change: Barriers and Solutions.

Global environmental changes induced by human activities are forcing organisms to respond at an unprecedented pace. At present we have only a limited understanding of why some species possess the capacity to respond to these changes while others do not. We introduce the concept of multidimensional phenospace as an organizing construct to understanding organismal evolutionary responses to environmental change. We then describe five barriers that currently challenge our ability to understand these responses: (1) Understanding the parameters of environmental change and their fitness effects, (2) Mapping and integrating phenotypic and genotypic variation, (3) Understanding whether changes in phenospace are heritable, (4) Predicting consistency of genotype to phenotype patterns across space and time, and (5) Determining which traits should be prioritized to understand organismal response to environmental change. For each we suggest one or more solutions that would help us surmount the barrier and improve our ability to predict, and eventually manipulate, organismal capacity to respond to anthropogenic change. Additionally, we provide examples of target species that could be useful to examine interactions between phenotypic plasticity and adaptive evolution in changing phenospace.

A machine learning approach for classifying and quantifying acoustic diversity.

1. Assessing diversity of discretely varying behavior is a classical ethological problem. In particular, the challenge of calculating an individuals' or species' vocal repertoire size is often an important step in ecological and behavioral studies, but a reproducible and broadly applicable method for accomplishing this task is not currently available. 2. We offer a generalizable method to automate the calculation and quantification of acoustic diversity using an unsupervised random forest framework. We tested our method using natural and synthetic datasets of known repertoire sizes that exhibit standardized variation in common acoustic features as well as in recording quality. We tested two approaches to estimate acoustic diversity using the output from unsupervised random forest analyses: (i) cluster analysis to estimate the number of discrete acoustic signals (e.g., repertoire size) and (ii) an estimation of acoustic area in acoustic feature space, as a proxy for repertoire size. 3. We find that our unsupervised analyses classify acoustic structure with high accuracy. Specifically, both approaches accurately estimate element diversity when repertoire size is small to intermediate (5-20 unique elements). However, for larger datasets (20-100 unique elements), we find that calculating the size of the area occupied in acoustic space is a more reliable proxy for estimating repertoire size. 4. We conclude that our implementation of unsupervised random forest analysis offers a generalizable tool that researchers can apply to classify acoustic structure of diverse datasets. Additionally, output from these analyses can be used to compare the distribution and diversity of signals in acoustic space, creating opportunities to quantify and compare the amount of acoustic variation among individuals, populations, or species in a standardized way. We provide R code and examples to aid researchers interested in using these techniques.

An integrative measure of cognitive performance, but not individual task performance, is linked to male reproductive output in budgerigars.

Cognitive abilities such as learning and memory are key for survival and reproduction. Individuals with high cognitive abilities may be more successful at attracting mates and producing offspring. However, empirical tests of and evidence supporting this hypothesis remain scarce. We measured cognitive performance of male budgerigars in four tasks: problem solving, detour reaching, seed discrimination, and spatial memory. We then tested female choice for male cognition at three stages of the mating choice process: social pairing, extra-pair mating, and continued reproductive investment with a social mate. We also measured female reproductive output. We used an integrative measure of male cognitive performance that encapsulates performance across all tasks, the 'composite cognitive score' by summing performance on the four tasks. In the first stage, females did not choose their social mates based on any of the measures of male cognitive performance. In the second stage, however, males with higher composite cognitive scores sired and raised more offspring. In the third stage, females increased their reproductive investment after the first breeding attempt when paired with males with higher detour-reaching scores. These results suggest that female reproductive decisions may shape overall male cognitive performance.

Defining the multidimensional phenotype: New opportunities to integrate the behavioral ecology and behavioral neuroscience of vocal learning.

Vocal learning has evolved independently in several lineages. This complex cognitive trait is commonly treated as binary: species either possess or lack it. This view has been a useful starting place to examine the origins of vocal learning, but is also incomplete and potentially misleading, as specific components of the vocal learning program - such as the timing, extent and nature of what is learned - vary widely among species. In our review we revive an idea first proposed by Beecher and Brenowitz (2005) by describing six dimensions of vocal learning: (1) which vocalizations are learned, (2) how much is learned, (3) when it is learned, (4) who it is learned from, (5) what is the extent of the internal template, and (6) how is the template integrated with social learning and innovation. We then highlight key examples of functional and mechanistic work on each dimension, largely from avian taxa, and discuss how a multi-dimensional framework can accelerate our understanding of why vocal learning has evolved, and how brains became capable of this important behaviour.

Social group signatures in hummingbird displays provide evidence of co-occurrence of vocal and visual learning.

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.

Swift declines predicted following mating system changes driven by an introduced predator.

In Focus: Heinsohn, R., Olah, G., Webb, M., Peakall, R., & Stojanovic, D. (2019). Sex ratio bias and shared paternity reduce individual fitness and population viability in a critically endangered parrot. Journal of Animal Ecology, 88, 502-510. While the effects of variation in the sex ratio of offspring have been thoroughly explored over the last century, the sex ratio of adults has received far less attention. A paper by Heinsohn and colleagues in this issue shows that changes in the adult sex ratio can have striking effects on mating systems, reproductive success and population viability. These impacts are all the more dramatic because they occur in a critically endangered species, the swift parrot, Lathamus discolor, of Tasmania. This species suffers heavy predation from the introduced sugar glider, Petaurus breviceps, which kills nesting females and their clutches, resulting in strongly male-biased adult sex ratios. The authors combined demographic and genetic data to show that, at sites with heavier predation, the remaining females were more likely to mate with multiple males. This shift in the mating system also led to lower overall nesting success, with fewer chicks fledged per nest at sites with higher levels of mixed paternity. Population viability models based on these data predicted steep population declines, with models using the highest observed rates of mixed paternity showing the sharpest declines. These results demonstrate that changes in the adult sex ratio can have far-reaching impacts, including on the fitness of populations themselves.

Does audience affect the structure of warble song in budgerigars (Melopsittacus undulatus)?

In many bird species, male song functions both to defend a territory against other males and to attract a female mate. Male budgerigars (Melopsittacus undulatus) produce a song-like vocal signal, the warble, that can be directed at either females or other males. Warble is a long, complex, low amplitude, and variable vocalization composed of different element types. While there is some evidence that warble can induce reproduction, the function of this signal is largely uncertain and it is unclear whether male- and female-directed warble differ in either function or structure. We recorded male budgerigars in the presence of either their mate or a familiar male to identify whether the warbles produced with different audiences differed in structure. We dissected each warble into specific element units, classified units into a limited number of types by rule-based visual classification and calculated the proportion of each element type, element diversity, and total duration for the male- and female-directed warbles of each male. We also examined the sequential organization of warble element types (syntax) using time-window lagged sequential analysis. We found no differences in the proportions of different elements used, element diversity or duration of warbles between male- and female-directed warble. The syntax of warbles is similar when directed at males or females. However, we found greater between-individual similarity in the sequential organization of warbles directed towards females than in those directed towards males. The greater syntactical consistency in female-directed warble suggests that females may prefer either specific types of element sequences, or consistency itself, and thus shape the organization of warbles.

Vocal dialects in parrots: patterns and processes of cultural evolution.

Vocal dialects have fascinated biologists for over 50 years. This mosaic pattern of geographic variation in learned vocalizations was first described in a songbird, and since that time, most studies investigating dialects have focused on songbird species. Here we examine patterns of geographic variation in the calls of a different group of vocal learning birds, the parrots (Order Psittaciformes). We summarize the growing literature on vocal variation in parrots, and complement this review with a survey of variation in the genus Amazona using calls from sound libraries. We find strikingly similar patterns to those previously found in songbirds. Over 90% of parrots examined in the literature, and 69% of Amazona species surveyed, showed geographic variation consistent with a propensity to share local call types. This trait is evolutionarily labile and widespread; within Amazona most clades contained species with and without geographic variation, and most major lineages of parrots include representatives with dialects. We found little support for the long-standing hypothesis that dialects isolate populations and thus generate genetic differences among populations. Instead, most studies support the idea that dialects are maintained by social benefits of matching local call types, a finding that has implications for the management of captive and endangered populations. Considerable scope remains for studies that experimentally test hypotheses for the exact nature of these benefits, as well as studies that employ comparisons among species, to understand how the interplay between ecology, social dynamics and vocal learning capacities produces different patterns of variation across the parrots.

Spatial memory is as important as weapon and body size for territorial ownership in a lekking hummingbird.

Advanced cognitive abilities have long been hypothesized to be important in mating. Yet, most work on sexual selection has focused on morphological traits and its relevance for cognitive evolution is poorly understood. We studied the spatial memory of lekking long-billed hermits (Phaethornis longirostris) and evaluated its role in lek territory ownership, the magnitude of its effect compared to phenotypic traits expected to influence sexual selection, and whether its variation is indicated in the structure of mating vocal signal. Spatial memory (the ability to recall the position of a rewarding feeder) was compared between "territorial" and "floater" males. Interestingly, although spatial memory and body size both positively affected the probability of lek territory ownership, our results suggest a stronger effect of spatial memory. Bill tip length (used as weapon in agonistic interactions) also showed a positive but smaller effect. Load lifting during vertical flight, a measure of physical performance relevant to agonistic interactions, had no effect on territory ownership. Finally, both body size and spatial memory were indicated in the structure of male song: body size negatively correlated with song lowest frequency, while spatial memory positively predicted song consistency. Together, our findings lend support for cognition as a sexual selection target.

Cognition, personality, and stress in budgerigars, Melopsittacus undulatus.

To study the fitness effects of individual variation in cognitive traits, it is paramount to understand whether traits such as personality and physiological stress influence cognitive performance. We first tested whether budgerigars showed both consistent personalities and cognitive performance across time and tasks. We tested object and food neophobia, and exploratory behavior. We measured cognitive performance in habituation, ability to solve foraging problems, spatial memory, and seed discrimination tasks. Budgerigars showed consistency in their neophobic tendencies and these tendencies were associated with their exploratory behavior. Birds were also consistent in how they performed in most of the cognitive tasks (temporal consistency), but were not consistent in their performance across tasks (context consistency). Neither corticosterone levels (baseline and stress-induced) showed a significant relationship with either cognitive or personality measures. Neophobic and exploratory tendencies determined the willingness of birds to engage only in the seed discrimination task. Such tendencies also had a significant effect on problem-solving ability. Our results suggest that consistent individual differences in cognitive performance along with consistent differences in personality could determine response to environmental change and therefore have important fitness consequences.

Social calls provide novel insights into the evolution of vocal learning.

Learned song is among the best-studied models of animal communication. In oscine songbirds, where learned song is most prevalent, it is used primarily for intrasexual selection and mate attraction. Learning of a different class of vocal signals, known as contact calls, is found in a diverse array of species, where they are used to mediate social interactions among individuals. We argue that call learning provides a taxonomically rich system for studying testable hypotheses for the evolutionary origins of vocal learning. We describe and critically evaluate four nonmutually exclusive hypotheses for the origin and current function of vocal learning of calls, which propose that call learning (1) improves auditory detection and recognition, (2) signals local knowledge, (3) signals group membership, or (4) allows for the encoding of more complex social information. We propose approaches to testing these four hypotheses but emphasize that all of them share the idea that social living, not sexual selection, is a central driver of vocal learning. Finally, we identify future areas for research on call learning that could provide new perspectives on the origins and mechanisms of vocal learning in both animals and humans.

Rearrangement and evolution of mitochondrial genomes in parrots.

Mitochondrial genome rearrangements that result in control region duplication have been described for a variety of birds, but the mechanisms leading to their appearance and maintenance remain unclear, and their effect on sequence evolution has not been explored. A recent survey of mitochondrial genomes in the Psittaciformes (parrots) found that control region duplications have arisen independently at least six times across the order. We analyzed complete mitochondrial genome sequences from 20 parrot species, including representatives of each lineage with control region duplications, to document the gene order changes and to examine effects of genome rearrangements on patterns of sequence evolution. The gene order previously reported for Amazona parrots was found for four of the six independently derived genome rearrangements, and a previously undescribed gene order was found in Prioniturus luconensis, representing a fifth clade with rearranged genomes; the gene order resulting from the remaining rearrangement event could not be confirmed. In all rearranged genomes, two copies of the control region are present and are very similar at the sequence level, while duplicates of the other genes involved in the rearrangement show signs of degeneration or have been lost altogether. We compared rates of sequence evolution in genomes with and without control region duplications and did not find a consistent acceleration or deceleration associated with the duplications. This could be due to the fact that most of the genome rearrangement events in parrots are ancient, and additionally, to an effect of body size on evolutionary rate that we found for mitochondrial but not nuclear sequences. Base composition analyses found that relative to other birds, parrots have unusually strong compositional asymmetry (AT- and GC-skew) in their coding sequences, especially at fourfold degenerate sites. Furthermore, we found higher AT skew in species with control region duplications. One potential cause for this compositional asymmetry is that parrots have unusually slow mtDNA replication. If this is the case, then any replicative advantage provided by having a second control region could result in selection for maintenance of both control regions once duplicated.

An RFID Based Smart Feeder for Hummingbirds.

We present an interdisciplinary effort to record feeding behaviors and control the diet of a hummingbird species (Phaethornis longirostris, the long-billed hermit or LBH) by developing a Radio Frequency Identification (RFID) based smart feeder. The system contains an RFID reader, a microcontroller, and a servo-controlled hummingbird feeder opener; the system is presented as a tool for studying the cognitive ability of the LBH species. When equipped with glass capsule RFID tags (which are mounted on the hummingbird), the smart feeder can provide specific diets for predetermined sets of hummingbirds at the discretion of biologists. This is done by reading the unique RFID tag on the hummingbirds and comparing the ID number with the pre-programmed ID numbers stored in the smart feeder. The smart feeder records the time and ID of each hummingbird visit. The system data is stored in a readily available SD card and is powered by two 9 V batteries. The detection range of the system is approximately 9-11 cm. Using this system, biologists can assign the wild hummingbirds to different experimental groups and monitor their diets to determine if they develop a preference to any of the available nectars. During field testing, the smart feeder system has demonstrated consistent detection (when compared to detections observed by video-recordings) of RFID tags on hummingbirds and provides pre-designed nectars varying water and sugar concentrations to target individuals. The smart feeder can be applied to other biological and environmental studies in the future.

Molecular phylogenetics suggests a New Guinean origin and frequent episodes of founder-event speciation in the nectarivorous lories and lorikeets (Aves: Psittaciformes).

The lories and lorikeets (Aves: Loriinae: Loriini) are a readily recognizable, discrete group of nectarivorous parrots confined to the Indo-Pacific region between Wallace's Line and the Pitcairn Island group in the central-east Pacific Ocean. We present the first phylogenetic analysis of all currently recognized genera in the group using two mitochondrial and five nuclear loci. Our analyses suggest a New Guinean origin for the group at about 10million years ago (95% HPD 4.8-14.8) but this origin must be interpreted within the context of that island's complicated, recent geological history. That is, the origin and early diversification of the group may have taken place as New Guinea's Central Cordillera arose and the final constituent terranes that form present-day New Guinea were accreted. The latter activity may have promoted dispersal as a key element in the group's history. We have detected several instances of dispersal out of New Guinea that we argue constitute instances of founder-event speciation. Some phenotypically cohesive genera are affirmed as monophyletic but other genera are clearly in need of taxonomic dismantlement and reclassification. We recognize Parvipsitta Mathews, 1916 for two species usually placed in Glossopsitta and we advocate transfer of Chalcopsitta cardinalis into Pseudeos Peters, 1935. Other non-monophyletic genera such as Charmosyna, Psitteuteles and, probably, Trichoglossus, require improved taxon sampling and further phylogenetic analysis before their systematics can be resolved. Cursory examination of trait mapping across the group suggests that many traits are ancestral and of little use in determining genus-level systematics.