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Ball, G. F.

Publications and source records attributed to Ball, G. F..

8 recordsLinked to original sources

Breeding Males, But Not Females, Have Elevated Androgen Receptor Expression in the Northern House Wren (Troglodytes Aedon), a Temperate Songbird with Female Song

In many male temperate-breeding songbirds, increased plasma testosterone in the early breeding season regenerates song control nuclei that regulate song. Females of some temperate species also sing but have lower circulating testosterone concentrations. We hypothesized that upregulation of steroid receptors in females could compensate for low circulating testosterone, focusing on the northern house wren (Troglodytes aedon), a temperate-breeding songbird in which both sexes sing. We collected brain tissue from both sexes during the early breeding, late breeding, and nonbreeding season. Using quantitative PCR, we quantified mRNA expression of four genes--androgen receptor (AR), estrogen receptors (ER and ER{beta}), and aromatase (AROM)--in three song nuclei--HVC, Area X, and RA--and compared sexes. We found females had lower expression than males of AR, AROM and ER in most song nuclei, especially of AR in HVC in the breeding season. Both sexes, however, had low ER expression in Area X and RA. In males, expression differed seasonally: breeding males had higher expression of AR in RA and AROM in HVC than nonbreeding males. In both sexes, expression differed among song nuclei: in most genes, HVC had the highest expression, followed by RA, then Area X. These findings suggest singing female house wrens do not compensate for low plasma testosterone by upregulating steroid receptors beyond male levels or during early breeding, when they sing most. Conversely, increased AR expression in breeding males indicates differences in the mechanisms regulating male and female song, with testosterone playing a greater role in male birdsong.

animal behavior and cognition↗

Seasonal neurogenomic changes provide genetic links between male song and testosterone-mediated neurogenesis in a wild songbird

Seasonal changes in testosterone mediate the transition from reduced singing in the non-breeding season to high song rates in the early breeding season in male temperate songbirds, a process accompanied by marked neurogenesis in song control regions of the brain. However, the resulting genetic changes and their association with the subsequent behavioral, neuroanatomical and reproductive changes remain poorly understood. Here, we compared gene expression in HVC, a major song control nucleus, between the non-breeding and breeding season in male northern house wrens (Troglodytes aedon) and we examined associations with HVC volume, plasma testosterone concentrations, and testes size. Differential gene expression analysis identified three genes (CLIP4, FAM169A, and TTR) consistently linked to seasonal transitions from non-breeding to three breeding stages (pre-laying, egg-laying and incubation). Notably, TTR, which transports thyroid hormone (TH), was highly expressed in the nonbreeding season, consistent with a possible role of TH in regulating seasonal shifts in song output and structure. We also identified seasonal changes in networks of genes related to neural connectivity, cellular restructuring, and cell migration. Weighted gene co-expression network analysis (WGCNA) revealed gene clusters specifically correlated with testosterone and HVC volume. Testosterone-associated genes included genes involved in neural circuit remodeling, chromatin organization, and cytoskeletal dynamics, consistent with testosterone-mediated regulation of these neuroanatomical changes. Genes linked to seasonal increases in HVC volume were involved in neuronal restructuring and neuron migration, implicating these genes in seasonal neurogenesis. Together, our findings link novel gene expression patterns to hormone regulation and neurogenesis underlying seasonal transitions in birdsong.

genomics↗

Does the syrinx, a peripheral structure, constrain effects of sex steroids on behavioral sex reversal in adult canaries?

We previously confirmed that effects of testosterone (T) on singing activity and on the volume of brain song control nuclei are sexually differentiated in adult canaries: females are limited in their ability to respond to T as males do. Here we expand on these results by focusing on sex differences in the production and performance of trills, i.e., rapid repetitions of song elements. We analyzed more than 42,000 trills recorded over a period of 6 weeks from 3 groups of castrated males and 3 groups of photoregressed females that received Silastic implants filled with T, T plus estradiol or left empty as control. Effects of T on the number of trills, trill duration and percent of time spent trilling were all stronger in males than females. Irrespective of endocrine treatment, trill performance assessed by vocal deviations from the trill rate versus trill bandwidth trade-off was also higher in males than in females. Finally, inter-individual differences in syrinx mass were positively correlated with trill production in males but not in females. Given that T increases syrinx mass and syrinx fiber diameter in males but not in females, these data indicate that sex differences in trilling behavior are related to sex differences in syrinx mass and syrinx muscle fiber diameter that cannot be fully reversed by sex steroids in adulthood. Sexual differentiation of behavior thus reflects organization not only of the brain but also of peripheral structures.

animal behavior and cognition↗

Unravelling the role of thyroid hormones in seasonal neuroplasticity in European Starlings (Sturnus vulgaris)

1Thyroid hormones clearly play a role in the seasonal regulation of reproduction, but any role they might play in song behavior and the associated seasonal neuroplasticity in songbirds remains to be elucidated. To pursue this question, we first established seasonal patterns in the expression of thyroid hormone regulating genes in male European starlings employing in situ hybridization methods. Thyroid hormone transporter LAT1 expression in the song nucleus HVC was elevated during the photosensitive phase, pointing towards an active role of thyroid hormones during this window of possible neuroplasticity. In contrast DIO3 expression was high in HVC during the photostimulated phase, limiting the possible effect of thyroid hormones to maintain song stability during the breeding season. Next, we studied the effect of hypothyroidism on song behavior and neuroplasticity using in vivo MRI. Hypothyroidism inhibited the photostimulation-induced increase in testosterone, confirming the role of thyroid hormones in activating the hypothalamic-pituitary-gonadal (HPG) axis. Surprisingly, apart from the myelination of several tracts during the photostimulated phase, most neuroplasticity related to song production was unaffected by hypothyroidism. Remarkably, T3 plasma concentrations were negatively correlated to the microstructural changes in several song control nuclei. Potentially, a global reduction of circulating thyroid hormones during the photosensitive period is necessary to lift the brake imposed by the photorefractory period, whereas local fine-tuning of thyroid hormone concentrations through LAT1 could activate underlying neuroplasticity mechanisms. Given the complexity of thyroid hormone effects, this study is a steppingstone to disentangle the influence of thyroid hormones on seasonal neuroplasticity.

neuroscience↗

Concurrent invasions by European starlings (Sturnus vulgaris) suggest selection on shared genomic regions even after genetic bottlenecks

A species success during the invasion of new areas hinges on an interplay between demographic processes and the outcome of localized selection. Invasive European Starlings (Sturnus vulgaris) established populations in Australia and North America in the 19th century. Here, we compare whole-genome sequences among native and independently introduced European Starling populations from three continents to determine how demographic processes interact with rapid adaptive evolution to generate similar genetic patterns in these recent and replicated invasions. Our results confirm that a post-bottleneck expansion may in fact support local adaptation. We find that specific genomic regions have differentiated even on this short evolutionary timescale, and suggest that selection best explains differentiation in at least two of these regions. This infamous and highly mobile invader adapted to novel selection (e.g., extrinsic factors), perhaps in part due to the demographic boom intrinsic to many invasions.

evolutionary biology↗

Perineuronal nets in HVC and plasticity in male canary song

Songbirds learn their vocalizations during developmental sensitive periods of song memorization and sensorimotor learning. Some seasonal songbirds, called open-ended learners, recapitulate transitions from sensorimotor learning and song crystallization on a seasonal basis during adulthood. In adult male canaries, sensorimotor learning occurs each year in autumn and leads to modifications of the syllable repertoire during successive breeding seasons. We previously showed that perineuronal nets (PNN) expression in song control nuclei decreases during this sensorimotor learning period. Here we explored the causal link between PNN expression in adult canaries and song modification by enzymatically degrading PNN in HVC, a key song control system nucleus. Three independent experiments identified limited effects of the PNN degradation in HVC on the song structure of male canaries. They clearly establish that presence of PNN in HVC is not required to maintain general features of crystallized song. Some suggestion was collected that PNN are implicated in the stability of song repertoires but this evidence is too preliminary to draw firm conclusions and additional investigations should consider producing PNN degradations at specified time points of the seasonal cycle. It also remains possible that once song has been crystallized at the beginning of the first breeding season, PNN no longer play a key role in determining song structure which could be tested by treatments with ChABC at key step in ontogeny. It would in this context be important to develop multiple stereotaxic procedures allowing the simultaneous bilateral degradation of PNN in several song control nuclei for extended periods.

neuroscience↗

Transcript- and annotation-guided genome assembly of the European starling

The European starling, Sturnus vulgaris, is an ecologically significant, globally invasive avian species that is also suffering from a major decline in its native range. Here, we present the genome assembly and long-read transcriptome of an Australian-sourced European starling (S. vulgaris vAU), and a second North American genome (S. vulgaris vNA), as complementary reference genomes for population genetic and evolutionary characterisation. S. vulgaris vAU combined 10x Genomics linked-reads, low-coverage Nanopore sequencing, and PacBio Iso-Seq full-length transcript scaffolding to generate a 1050 Mb assembly on 1,628 scaffolds (72.5 Mb scaffold N50). Species-specific transcript mapping and gene annotation revealed high structural and functional completeness (94.6% BUSCO completeness). Further scaffolding against the high-quality zebra finch (Taeniopygia guttata) genome assigned 98.6% of the assembly to 32 putative nuclear chromosome scaffolds. Rapid, recent advances in sequencing technologies and bioinformatics software have highlighted the need for evidence-based assessment of assembly decisions on a case-by-case basis. Using S. vulgaris vAU, we demonstrate how the multifunctional use of PacBio Iso-Seq transcript data and complementary homology-based annotation of sequential assembly steps (assessed using a new tool, SAAGA) can be used to assess, inform, and validate assembly workflow decisions. We also highlight some counter-intuitive behaviour in traditional BUSCO metrics, and present BO_SCPLOWUSCOMPC_SCPLOW, a complementary tool for assembly comparison designed to be robust to differences in assembly size and base-calling quality. Finally, we present a second starling assembly, S. vulgaris vNA, to facilitate comparative analysis and global genomic research on this ecologically important species.

genomics↗

Monogamy in a moment: how do brief social interactions change over time in pair-bonded zebra finches (Taeniopygia guttata)?

Research on monogamy has largely focused on marked behaviors that are unique to pair bonded partners. However, these marked behaviors represent only a subset of the pair-directed behaviors that partners engage in; the influence of pair bonding on mundane or subtle social interactions among partners remains largely unknown. In the current study, we describe the changes that occur during brief social reunions (or greets) over the course of pair bonding in zebra finches. We quantified pair-directed behavior during five-minute reunions from three stages of pair bonding: initial pairing (between 4-72 hrs), early pairing (1-2 weeks) and late pairing (>1 month). These social interactions were operationalized in multiples ways. First, we quantified the overall activity levels (call and movement rates) for both the male and female. Overall, females were more active than males, but for both males and females calling activity was highest during the initial timepoint (between 4-72 hrs post-pairing). We quantified behavioral coordination between partners in two ways, 1) similarity in call and movement rates between partners, and 2) temporal synchrony between calls and movements (via sliding correlation coefficients of time-stamped calls and movements). Overall there were no effects of pairing on behavioral coordination. Finally, we used principal component analyses to disentangle behavioral coordination from the activity levels of the male and female. These results contribute to a growing line of evidence that male and female zebra finches differentially contribute to social dynamics and highlight the influence of pair bonding on the development of social dynamics. Behavioral coordination is clearly important for marked interactions (e.g. duetting, courtship displays and biparental care). Our results raise the question of what the roles of such mundane social interactions are in monogamous partnerships.Competing Interest StatementThe authors have declared no competing interest.View Full Text

animal behavior and cognition↗