Jean-Nicolas Audet

Convergent differential regulation of SLIT-ROBO axon guidance genes in the brains of vocal learners

Only a few distantly related mammals and birds have the trait of complex vocal learning, which is the ability to imitate novel sounds. This ability is critical for speech acquisition and production in humans, and is attributed to specialized forebrain vocal control circuits that have several unique connections relative to adjacent brain circuits. As a result, it has been hypothesized that there could exist convergent changes in genes involved in neural connectivity of vocal learning circuits. In support of this hypothesis, expanding on our related study (Pfenning et al. [2014] Science 346: 1256846), here we show that the forebrain part of this circuit that makes a relatively rare direct connection to brainstem vocal motor neurons in independent lineages of vocal learning birds (songbird, parrot, and hummingbird) has specialized regulation of axon guidance genes from the SLIT–ROBO molecular pathway. The SLIT1 ligand was differentially downregulated in the motor song output nucleus that makes the direct projection, whereas its receptor ROBO1 was developmentally upregulated during critical periods for vocal learning. Vocal nonlearning bird species and male mice, which have much more limited vocal plasticity and associated circuits, did not show comparable specialized regulation of SLIT–ROBO genes in their nonvocal motor cortical regions. These findings are consistent with SLIT and ROBO gene dysfunctions associated with autism, dyslexia, and speech sound language disorders and suggest that convergent evolution of vocal learning was associated with convergent changes in the SLIT–ROBO axon guidance pathway. J. Comp. Neurol. 523:892–906, 2015.

Problem-solving and learning in Carib grackles: individuals show a consistent speed–accuracy trade-off

AbstractThe generation and maintenance of within-population variation in cognitive abilities remain poorly understood. Recent theories propose that this variation might reflect the existence of consistent cognitive strategies distributed along a slow–fast continuum influenced by shyness. The slow–fast continuum might be reflected in the well-known speed–accuracy trade-off, where animals cannot simultaneously maximise the speed and the accuracy with which they perform a task. We test this idea on 49 wild-caught Carib grackles (Quiscalus lugubris), a tame opportunistic generalist Icterid bird in Barbados. Grackles that are fast at solving novel problems involving obstacle removal to reach visible food perform consistently over two different tasks, spend more time per trial attending to both tasks, and are those that show more shyness in a pretest. However, they are also the individuals that make more errors in a colour discrimination task requiring no new motor act. Our data reconcile some of the mixed positive and negative correlations reported in the comparative literature on cognitive tasks, suggesting that a speed–accuracy trade-off could lead to negative correlations between tasks favouring speed and tasks favouring accuracy, but still reveal consistent strategies based on stable individual differences.

De novo PacBio long-read and phased avian genome assemblies correct and add to reference genes generated with intermediate and short reads.

Abstract Reference-quality genomes are expected to provide a resource for studying gene structure, function, and evolution. However, often genes of interest are not completely or accurately assembled, leading to unknown errors in analyses or additional cloning efforts for the correct sequences. A promising solution is long-read sequencing. Here we tested PacBio-based long-read sequencing and diploid assembly for potential improvements to the Sanger-based intermediate-read zebra finch reference and Illumina-based short-read Annas hummingbird reference, 2 vocal learning avian species widely studied in neuroscience and genomics. With DNA of the same individuals used to generate the reference genomes, we generated diploid assemblies with the FALCON-Unzip assembler, resulting in contigs with no gaps in the megabase range, representing 150-fold and 200-fold improvements over the current zebra finch and hummingbird references, respectively. These long-read and phased assemblies corrected and resolved what we discovered to be numerous misassemblies in the references, including missing sequences in gaps, erroneous sequences flanking gaps, base call errors in difficult-to-sequence regions, complex repeat structure errors, and allelic differences between the 2 haplotypes. These improvements were validated by single long-genome and transcriptome reads and resulted for the first time in completely resolved protein-coding genes widely studied in neuroscience and specialized in vocal learning species. These findings demonstrate the impact of long reads, sequencing of previously difficult-to-sequence regions, and phasing of haplotypes on generating the high-quality assemblies necessary for understanding gene structure, function, and evolution.

Feeding innovations in a nested phylogeny of Neotropical passerines

Several studies on cognition, molecular phylogenetics and taxonomic diversity independently suggest that Darwins finches are part of a larger clade of speciose, flexible birds, the family Thraupidae, a member of the New World nine-primaried oscine superfamily Emberizoidea. Here, we first present a new, previously unpublished, dataset of feeding innovations covering the Neotropical region and compare the stem clades of Darwins finches to other neotropical clades at the levels of the subfamily, family and superfamily/order. Both in terms of raw frequency as well as rates corrected for research effort and phylogeny, the family Thraupidae and superfamily Emberizoidea show high levels of innovation, supporting the idea that adaptive radiations are favoured when the ancestral stem species were flexible. Second, we discuss examples of innovation and problem-solving in two opportunistic and tame Emberizoid species, the Barbados bullfinch Loxigilla barbadensis and the Carib grackle Quiscalus lugubris fortirostris in Barbados. We review studies on these two species and argue that a comparison of L. barbadensis with its closest, but very shy and conservative local relative, the black-faced grassquit Tiaris bicolor, might provide key insights into the evolutionary divergence of cognition.

What’s flexible in behavioral flexibility?

Lay SummaryBehavioral flexibility is measured using a plethora of non-equivalent tasks. In experimental psychology, tests include reversal learning, set-shifting and self-control tasks. In addition to the latter tasks, behavioral ecologists have measured behavioral flexibility with tasks that include problem-solving and personality tests. A relationship between behavioral flexibility assessments, especially in behavioral ecology, still needs to be demonstrated. We argue that using a single umbrella term that incorporates too many unrelated traits should be avoided.

Innovativeness and the effects of urbanization on risk-taking behaviors in wild Barbados birds

The effects of urbanization on avian cognition remain poorly understood. Risk-taking behaviors like boldness, neophobia and flight distance are thought to affect opportunism and innovativeness, and should also vary with urbanization. Here, we investigate variation in risk-taking behaviors in the field in an avian assemblage of nine species that forage together in Barbados and for which innovation rate is known from previous work. We predicted that birds from highly urbanized areas would show more risk-taking behavior than conspecifics from less urbanized parts of the island and that the differences would be strongest in the most innovative of the species. Overall, we found that urban birds are bolder, less neophobic and have shorter flight distances than their less urbanized conspecifics. Additionally, we detected between-species differences in the effect of urbanization on flight distance, more innovative species showing smaller differences in flight distance between areas. Our results suggest that, within successful urban colonizers, species differences in innovativeness may affect the way species change their risk-taking behaviors in response to the urban environment.

Morphological and Molecular Sexing of the Monochromatic Barbados Bullfinch, Loxigilla barbadensis

The bullfinch Loxigilla barbadensis is an endemic passerine on the Caribbean island of Barbados that has only recently been taxonomically split from the Lesser Antillean bullfinch L. noctis. The trait that most clearly distinguishes L. barbadensis from L. noctis is the absence in the male of sexually dimorphic coloration of the body and throat feathers, with L. barbadensis males and females sharing the same dull brown plumage. Here we report, in 64 individuals netted throughout the island, the results of a discriminant analysis on two (wing length and tail length) to four morphological traits showing very high (97%) concordance with sexing via PCR using blood samples. Females also show a paler lower mandible, a trait that yields an 80% concordance with PCR sexing. We found one L. barbadensis male that had a noctis-like reddish throat patch, supporting the idea that sexual dichromatism is the ancestral condition and that male Barbados bullfinches have evolved cryptic coloration that now makes the species monochromatic.

Divergence in problem-solving skills is associated with differential expression of glutamate receptors in wild finches

Wild birds that vary in their problem-solving capacity were found to express different neurotransmitter receptor densities. Problem solving and innovation are key components of intelligence. We compare wild-caught individuals from two species that are close relatives of Darwin’s finches, the innovative Loxigilla barbadensis, and its most closely related species in Barbados, the conservative Tiaris bicolor. We found an all-or-none difference in the problem-solving capacity of the two species. Brain RNA sequencing analyses revealed interspecific differences in genes related to neuronal and synaptic plasticity in the intrapallial neural populations (mesopallium and nidopallium), especially in the nidopallium caudolaterale, a structure functionally analogous to the mammalian prefrontal cortex. At a finer scale, we discovered robust differences in glutamate receptor expression between the species. In particular, the GRIN2B/GRIN2A ratio, known to correlate with synaptic plasticity, was higher in the innovative L. barbadensis. These findings suggest that divergence in avian intelligence is associated with similar neuronal mechanisms to that of mammals, including humans.

Bajan Birds Pull Strings: Two Wild Antillean Species Enter the Select Club of String-Pullers

String-pulling is one of the most popular tests in animal cognition because of its apparent complexity, and of its potential to be applied to very different taxa. In birds, the basic procedure involves a food reward, suspended from a perch by a string, which can be reached by a series of coordinated pulling actions with the beak and holding actions of the pulled lengths of string with the foot. The taxonomic distribution of species that pass the test includes several corvids, parrots and parids, but in other families, data are much spottier and the number of individuals per species that succeed is often low. To date, the association between string-pulling ability and other cognitive traits was never tested. It is generally assumed that string-pulling is a complex form of problem-solving, suggesting that performance on string-pulling and other problem-solving tasks should be correlated. Here, we show that individuals of two innovative species from Barbados, the bullfinch Loxigilla barbadensis and the Carib grackle Quiscalus lugubris fortirostris, pass the string-pulling test. Eighteen of the 42 bullfinches tested succeeded, allowing us to correlate performance on this test to that on several other behavioral measurements. Surprisingly, string-pulling in bullfinches was unrelated to shyness, neophobia, problem-solving, discrimination and reversal learning performance. Only two of 31 grackles tested succeeded, precluding correlational analyses with other measures but still, the two successful birds largely differed in their other behavioral traits.