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Clayton, D. F.

Publications and source records attributed to Clayton, D. F..

6 recordsLinked to original sources

Multiome Profiling Reveals Astrocyte and Neuroendocrine Targets of Prenatal Acoustic Programming in Zebra Finch Embryos

Climate change is driving more frequent and severe heat events, yet the developmental mechanisms by which organisms anticipate and adapt to thermal stress remain poorly understood. In zebra finches (Taeniopygia guttata), parents exposed to extreme heat emit distinctive "heat call" vocalizations during late incubation that trigger adaptive phenotypic responses in offspring, including altered growth, thermoregulation, and reproductive success. Recent transcriptomic analysis revealed that prenatal heat call exposure induces hypothalamic gene expression changes enriched in non-neuronal populations, but cellular heterogeneity has obscured which cell types are primary targets and the regulatory mechanisms underlying acoustic programming. Here, we performed single-nucleus multiome sequencing to generate a cell-type-resolved atlas of gene expression and chromatin accessibility in the late-stage embryonic zebra finch hypothalamus. We find that heat call exposure selectively remodels astrocyte regulatory landscapes, with most playback-responsive chromatin changes localized to glial populations like astrocytes, challenging neuron-centric models of developmental programming. Motif enrichment and gene regulatory network analysis showed Nuclear Factor I-C, AP-1, and Notch pathway components - canonical drivers of the gliogenic switch - coordinate this response. Chromatin co-accessibility analysis revealed extensive astrocyte-specific enhancer-promoter rewiring at developmental signaling hubs, and pseudotemporal analysis identified condition-associated shifts in developmental trajectories and astrocyte gene-expression dynamics consistent with altered gliogenic programs. In parallel, we identified sex-dimorphic regulation of transthyretin in glutamatergic neurons of the paraventricular nucleus, linking acoustic programming to thyroid-dependent neuroendocrine pathways. These findings suggest that prenatal acoustic experience engages astrocyte-selective epigenetic priming and neuroendocrine transcriptional responses that may reshape hypothalamic developmental programs under predicted thermal environments.

developmental biology↗

Programming of Embryonic Blood Brain Barrier and Neurovascular Transcriptome by an Anticipatory Acoustic Signal of Heat in the Zebra Finch

AbstractOrganisms have evolved mechanisms to adjust to rapid environmental change. A dramatic example is the Australian zebra finch, where incubating parents produce an acoustic signal ("heat call") during extreme heat, triggering adaptive phenotypic plasticity in their offspring growth, thermoregulation, and reproductive success. To elucidate for the first time the molecular mechanisms underlying heat call-induced programming, we hypothesized a prenatal shift in hypothalamic gene expression, given the hypothalamuss central role in neuroendocrine signaling controlling metabolism and growth. In addition, we tested whether prenatal heat-call exposure induces local changes in the brain, to protect this highly heat-sensitive organ from upcoming heat challenges. We exposed zebra finch embryos to chronic playback of parental heat calls or control calls, then isolated the hypothalamus for RNA sequencing to identify differentially expressed genes and gene regulatory networks. Heat-call exposure elicited modest neuroendocrine gene expression changes, but robust downregulation of genes tied to muscle contraction and cytoskeletal dynamics, with evidence of isoform usage shifts. These changes were prominently localized to hypothalamic neurovascular endothelial, mural, and ependymal cell populations, forming the blood-brain barrier (BBB). Because embryos experienced heat-associated sound, but not heat itself, and changes matched the loosening of the BBB to avoid breakages, these transcriptomic shifts likely represent an anticipatory response to enhance subsequent brain resilience to heat. Our study provides the first genome-wide characterization of embryonic hypothalamic gene expression in a songbird and reveals that prenatal acoustic cues can developmentally program neurovascular systems, expanding current understanding of developmental plasticity under climate change.

developmental biology↗

Bird song comparison using deep learning trained from avian perceptual judgments

Our understanding of bird song, a model system for animal communication and the neurobiology of learning, depends critically on making reliable, validated comparisons between the complex multidimensional syllables that are used in songs. However, most assessments of song similarity are based on human inspection of spectrograms, or computational methods developed from human intuitions. Using a novel automated operant conditioning system, we collected a large corpus of zebra finches (Taeniopygia guttata) decisions about song syllable similarity. We use this dataset to compare and externally validate similarity algorithms in widely-used publicly available software (Raven, Sound Analysis Pro, Luscinia). Although these methods all perform better than chance, they do not closely emulate the avian assessments. We then introduce a novel deep learning method that can produce perceptual similarity judgements trained on such avian decisions. We find that this new method outperforms the established methods in accuracy and more closely approaches the avian assessments. Inconsistent (hence ambiguous) decisions are a common occurrence in animal behavioural data; we show that a modification of the deep learning training that accommodates these leads to the strongest performance. We argue this approach is the best way to validate methods to compare song similarity, that our dataset can be used to validate novel methods, and that the general approach can easily be extended to other species.

animal behavior and cognition↗

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↗

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↗

The variability of song variability in wild and domesticated zebra finches Taeniopygia guttata

Birdsong is a classic example of a learned social behavior. Like many traits of interest, however, song production is also influenced by genetic factors and understanding the relative contributions of genetic and environmental influences remains a major research goal. In this study we take advantage of genetic variation among captive zebra finch populations to examine variation in a population-level song trait: song variability. We find that zebra finch populations differ in levels of song variability. Domesticated T. g. castanotis populations displayed higher song diversity than more recently wild-derived populations of both zebra finch subspecies T. g. castanotis and T. g. guttata, the Timor zebra finch. To determine whether these differences could have a genetic basis, we cross-fostered domesticated T. g. castanotis and Timor zebra finches to Bengalese finches Lonchura striata domestica. Following cross-fostering, domesticated T. g. castanotis maintained a higher level of song diversity than T. g. guttata. We suggest that the high song variability of domesticated zebra finches may be a consequence of reduced purifying selection acting on song traits. Intraspecific differences in the mechanisms underlying song variability therefore represent an untapped opportunity for probing the mechanisms of song learning and production.

animal behavior and cognition↗