Brain transcriptome sequencing and assembly of three songbird model systems for the study of social behavior

Balakrishnan, Christopher N.; Mukai, Motoko; Gonser, Rusty A.; Wingfield, John C.; London, Sarah E.; Tuttle, Elaina M.; Clayton, David F.

doi:10.7717/peerj.396

Cited by 33 publications

(21 citation statements)

References 49 publications

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“…To investigate the long-term evolutionary history of chromosomes 2 and 2 m , we examined genome-wide patterns of divergence between the white-throated sparrow and its close relatives. For comparison, we analyzed closely-related taxa with previously [16, 17] or newly sequenced transcriptomes or genomes (Figure 1B). As in previous studies [11], we find that the relationship of chromosomes 2 and 2 m conflicts with the species tree and suggests more recent common ancestry of chromosome 2 with other taxa than with 2 m .…”

Section: Resultsmentioning

confidence: 99%

Divergence and Functional Degradation of a Sex Chromosome-like Supergene

et al. 2016

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SUMMARY A major challenge in biology is to understand the genetic basis of adaptation. One compelling idea is that groups of tightly linked genes (i.e. ‘supergenes’ [1, 2]) facilitate adaptation in suites of traits that determine fitness. Despite their likely importance, little is known about how alternate supergene alleles arise and become differentiated, nor their ultimate fate within species. Herein we address these questions by investigating the evolutionary history of a supergene in white-throated sparrows, Zonotrichia albicollis. This species comprises two morphs, tan and white, that differ in pigmentation and components of social behavior [3–5]. Morph is determined by alternative alleles at a balanced >100Mb inversion-based supergene, providing a unique system for studying gene-behavior relationships. Using over two decades of field data we document near-perfect disassortative mating among morphs, as well as the fitness consequences of rare assortative mating. We use de novo whole genome sequencing coupled with population- and phylo-genomic data, to show that alternate supergene alleles are highly divergent at over 1,000 genes, that these alleles originated prior to the split of Z. albicollis from its sister species, and may be polymorphic in Z. albicollis due to a past hybridization event. We provide evidence that the ‘white' allele may be degrading, similar to neo-Y/Wsex chromosomes. We further show that the ‘tan’ allele has surprisingly low levels of genetic diversity, yet does not show several canonical signatures of recurrent positive selection. We discuss these results in the context of the origin, molecular evolution, and possible fate of this remarkable polymorphism.

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Section: Resultsmentioning

confidence: 99%

Divergence and Functional Degradation of a Sex Chromosome-like Supergene

et al. 2016

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“…Additionally, we identified morphspecific gene expression driven by innate immunity genes and genes located in the chromosome 2 inversion. As adults, the genes within the inversion strongly influence the WTSP neural transcriptome (Balakrishnan et al, 2014;Zinzow-Kramer et al, 2015). Our results here suggest that as nestlings, parental genotypes and associated behaviours, rather than nestling genotype, have the strongest influence on the nestling transcriptome.…”

Section: Wgcna: Pair Typementioning

confidence: 69%

Parent and offspring genotypes influence gene expression in early life

et al. 2019

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Parents can have profound effects on offspring fitness. Little, however, is known about the mechanisms through which parental genetic variation influences offspring physiology in natural systems. White‐throated sparrows (Zonotrichia albicollis, WTSP) exist in two genetic morphs, tan and white, controlled by a large polymorphic supergene. Morphs mate disassortatively, resulting in two pair types: tan male × white female (T × W) pairs, which provide biparental care and white male × tan female (W × T) pairs, which provide female‐biased care. To investigate how parental composition impacts offspring, we performed RNA‐seq on whole blood of WTSP nestlings sampled from nests of both pair types. Parental pair type had a large effect on nestling gene expression, with 881 genes differentially expressed (DE) and seven correlated gene coexpression modules. The DE genes and modules expressed at higher levels in W × T nests with female‐biased parental care function in metabolism and stress‐related pathways resulting from the overrepresentation of proteolysis and stress‐response genes (e.g., SOD2, NR3C1). These results show that parental genotypes and/or associated behaviours influence nestling physiology, and highlight avenues of further research investigating the ultimate implications for the maintenance of this polymorphism. Nestlings also exhibited morph‐specific gene expression, with 92 differentially expressed genes, comprising immunity genes and genes encompassed by the supergene. Remarkably, we identified the same regulatory hub genes in these blood‐derived expression networks as were previously identified in adult WTSP brains (EPM2A, BPNT1, TAF5L). These hub genes were located within the supergene, highlighting the importance of this gene complex in structuring regulatory networks across diverse tissues.

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“…Left- and right-handedness in cichlid fish, for example, is correlated strongly with hemispheric and regional asymmetry of gene expression [241]. In songbirds, clustering analyses performed on retrieved sets of genes demonstrate a strong association of gene expression with brain region [25, 96, 359]. This also holds true for mammalian brain.…”

Section: Why Does Location Matter?mentioning

confidence: 99%