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result(s) for
"Christopher N. Balakrishnan"
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Stable recombination hotspots in birds
2015
The DNA-binding protein PRDM9 has a critical role in specifying meiotic recombination hotspots in mice and apes, but it appears to be absent from other vertebrate species, including birds. To study the evolution and determinants of recombination in species lacking the gene that encodes PRDM9, we inferred fine-scale genetic maps from population resequencing data for two bird species: the zebra finch, Taeniopygia guttata, and the long-tailed finch, Poephila acuticauda. We found that both species have recombination hotspots, which are enriched near functional genomic elements. Unlike in mice and apes, most hotspots are shared between the two species, and their conservation seems to extend over tens of millions of years. These observations suggest that in the absence of PRDM9, recombination targets functional features that both enable access to the genome and constrain its evolution.
Journal Article
Comparative transcriptome analysis of Indian domestic duck reveals candidate genes associated with egg production
by
Foote, Dustin J.
,
Balakrishnan, Christopher N.
,
Singha, Hijam Surachandra
in
631/208/212/2019
,
631/92/500
,
Aquatic birds
2022
Egg production is an important economic trait and a key indicator of reproductive performance in ducks. Egg production is regulated by several factors including genes. However the genes involved in egg production in duck remain unclear. In this study, we compared the ovarian transcriptome of high egg laying (HEL) and low egg laying (LEL) ducks using RNA-Seq to identify the genes involved in egg production. The HEL ducks laid on average 433 eggs while the LEL ducks laid 221 eggs over 93 weeks. A total of 489 genes were found to be significantly differentially expressed out of which 310 and 179 genes were up and downregulated, respectively, in the HEL group. Thirty-eight differentially expressed genes (DEGs), including
LHX9, GRIA1, DBH, SYCP2L, HSD17B2, PAR6, CAPRIN2, STC2,
and
RAB27B
were found to be potentially related to egg production and folliculogenesis. Gene ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analysis suggested that DEGs were enriched for functions related to glutamate receptor activity, serine-type endopeptidase activity, immune function, progesterone mediated oocyte maturation and MAPK signaling. Protein–protein interaction network analysis (PPI) showed strong interaction between 32 DEGs in two distinct clusters. Together, these findings suggest a mix of genetic and immunological factors affect egg production, and highlights candidate genes and pathways, that provides an understanding of the molecular mechanisms regulating egg production in ducks and in birds more broadly.
Journal Article
Gene expression in male and female stickleback from populations with convergent and divergent throat coloration
by
Balakrishnan, Christopher N.
,
McKinnon, Jeffrey S.
,
Newsome, William Burns
in
Behavioural Ecology
,
carotenoid
,
Carotenoids
2022
Understanding of genetic mechanisms underlying variation in sexual dichromatism remains limited, especially for carotenoid‐based colors. We addressed this knowledge gap in a gene expression study with threespine stickleback. We compared male and female throat tissues across five populations, including two in which female red coloration has evolved convergently. We found that the expression of individual genes, gene ontologies, and coexpression networks associated with red female color within a population differed between California and British Columbia populations, suggesting differences in underlying mechanisms. Comparing females from each of these populations to females from populations dominated by dull females, we again found extensive expression differences. For each population, genes and networks associated with female red color showed the same patterns for males only inconsistently. The functional roles of genes showing correlated expression with female color are unclear within populations, whereas genes highlighted through inter‐population comparisons include some previously suggested to function in carotenoid pathways. Among these, the most consistent patterns involved TTC39B (Tetratricopeptide Repeat Domain 39B), which is within a known red coloration QTL in stickleback and implicated in red coloration in other taxa. Understanding of genetic mechanisms mediating variation in sexual dichromatism remains limited, especially for carotenoid‐based colors. Comparing gene expression in skin tissue from five populations of stickleback, including two in which female red coloration has evolved convergently, we found extensive inter‐population differences in the genes showing red‐correlated expression in females. Nevertheless, TTC39B, which has been suggested to mediate carotenoid‐based coloration in several taxa and is located within a stickleback pigmentation QTL, was consistently associated with red throat color.
Journal Article
Nucleotide Variation, Linkage Disequilibrium and Founder-Facilitated Speciation in Wild Populations of the Zebra Finch (Taeniopygia guttata)
by
Edwards, Scott V
,
Balakrishnan, Christopher N
in
Animals
,
Animals, Wild - anatomy & histology
,
Animals, Wild - classification
2009
The zebra finch has long been an important model system for the study of vocal learning, vocal production, and behavior. With the imminent sequencing of its genome, the zebra finch is now poised to become a model system for population genetics. Using a panel of 30 noncoding loci, we characterized patterns of polymorphism and divergence among wild zebra finch populations. Continental Australian populations displayed little population structure, exceptionally high levels of nucleotide diversity (π = 0.010), a rapid decay of linkage disequilibrium (LD), and a high population recombination rate (ρ ≈ 0.05), all of which suggest an open and fluid genomic background that could facilitate adaptive variation. By contrast, substantial divergence between the Australian and Lesser Sunda Island populations (KST = 0.193), reduced genetic diversity (π = 0.002), and higher levels of LD in the island population suggest a strong but relatively recent founder event, which may have contributed to speciation between these populations as envisioned under founder-effect speciation models. Consistent with this hypothesis, we find that under a simple quantitative genetic model both drift and selection could have contributed to the observed divergence in six quantitative traits. In both Australian and Lesser Sundas populations, diversity in Z-linked loci was significantly lower than in autosomal loci. Our analysis provides a quantitative framework for studying the role of selection and drift in shaping patterns of molecular evolution in the zebra finch genome.
Journal Article
Dynamic molecular evolution of a supergene with suppressed recombination in white-throated sparrows
by
Jeong, Hyeonsoo
,
Layman, Thomas S
,
Chatterjee, Paramita
in
Animals
,
evolution
,
Evolution, Molecular
2022
In white-throated sparrows, two alternative morphs differing in plumage and behavior segregate with a large chromosomal rearrangement. As with sex chromosomes such as the mammalian Y, the rearranged version of chromosome two (ZAL2 m ) is in a near-constant state of heterozygosity, offering opportunities to investigate both degenerative and selective processes during the early evolutionary stages of ‘supergenes.’ Here, we generated, synthesized, and analyzed extensive genome-scale data to better understand the forces shaping the evolution of the ZAL2 and ZAL2 m chromosomes in this species. We found that features of ZAL2 m are consistent with substantially reduced recombination and low levels of degeneration. We also found evidence that selective sweeps took place both on ZAL2 m and its standard counterpart, ZAL2, after the rearrangement event. Signatures of positive selection were associated with allelic bias in gene expression, suggesting that antagonistic selection has operated on gene regulation. Finally, we discovered a region exhibiting long-range haplotypes inside the rearrangement on ZAL2 m . These haplotypes appear to have been maintained by balancing selection, retaining genetic diversity within the supergene. Together, our analyses illuminate mechanisms contributing to the evolution of a young chromosomal polymorphism, revealing complex selective processes acting concurrently with genetic degeneration to drive the evolution of supergenes.
Journal Article
Gene Regulatory Evolution During Speciation in a Songbird
2016
Over the last decade, tremendous progress has been made toward a comparative understanding of gene regulatory evolution. However, we know little about how gene regulation evolves in birds, and how divergent genomes interact in their hybrids. Because of the unique features of birds – female heterogamety, a highly conserved karyotype, and the slow evolution of reproductive incompatibilities – an understanding of regulatory evolution in birds is critical to a comprehensive understanding of regulatory evolution and its implications for speciation. Using a novel complement of analyses of replicated RNA-seq libraries, we demonstrate abundant divergence in brain gene expression between zebra finch (Taeniopygia guttata) subspecies. By comparing parental populations and their F1 hybrids, we also show that gene misexpression is relatively rare among brain-expressed transcripts in male birds. If this pattern is consistent across tissues and sexes, it may partially explain the slow buildup of postzygotic reproductive isolation observed in birds relative to other taxa. Although we expected that the action of genetic drift on the island-dwelling zebra finch subspecies would be manifested in a higher rate of trans regulatory divergence, we found that most divergence was in cis regulation, following a pattern commonly observed in other taxa. Thus, our study highlights both unique and shared features of avian regulatory evolution.
Journal Article
Susceptibility and Antibody Response of the Laboratory Model Zebra Finch (Taeniopygia guttata) to West Nile Virus
by
Hofmeister, Erik K.
,
Shearn-Bochsler, Valerie
,
Balakrishnan, Christopher N.
in
Analysis
,
Animal behavior
,
Animal models
2017
Since the introduction of West Nile virus (WNV) into North America in 1999 a number of passerine bird species have been found to play a role in the amplification of the virus. Arbovirus surveillance, observational studies and experimental studies have implicated passerine birds (songbirds, e.g., crows, American robins, house sparrows, and house finches) as significant reservoirs of WNV in North America, yet we lack a tractable passerine animal model for controlled studies of the virus. The zebra finch (Taeniopygia guttata) serves as a model system across a diversity of fields, and here we develop the zebra finch a songbird model for WNV. Like many natural hosts of WNV, we found that zebra finches developed sufficient viremia to serve as a competent host, yet in general resisted mortality from infection. In the Australian zebra finch (AZF) T. g. castanotis, we detected WNV in the majority of sampled tissues by 4 days post injection (dpi). However, WNV was not detected in tissues of sacrificed birds at 14 dpi, shortly after the development of detectable anti-WNV antibodies in the majority of birds indicating successful viral clearance. We compared susceptibility between the two zebra finch subspecies AZF and Timor zebra finch (TZF) T. g. guttata. Compared to AZF, WNV RNA was detected in a larger proportion of challenged TZF and molecular detection of virus in the serum of TZF was significantly higher than in AZF. Given the observed moderate host competence and disease susceptibility, we suggest that zebra finches are appropriate as models for the study of WNV and although underutilized in this respect, may be ideal models for the study of the many diseases carried and transmitted by songbirds.
Journal Article
Speciation in Birds: Genes, Geography, and Sexual Selection
by
Balakrishnan, Christopher N.
,
Swanson, Willie J.
,
Kingan, Sarah B.
in
Animals
,
Aves
,
Biological taxonomies
2005
Molecular studies of speciation in birds over the last three decades have been dominated by a focus on the geography, ecology, and timing of speciation, a tradition traceable to Mayr's Systematics and the Origin of Species. However, in the recent years, interest in the behavioral and molecular mechanisms of speciation in birds has increased, building in part on the older traditions and observations from domesticated species. The result is that many of the same mechanisms proffered for model lineages such as Drosophila-mechanisms such as genetic incompatibilities, reinforcement, and sexual selection-are now being seriously entertained for birds, albeit with much lower resolution. The recent completion of a draft sequence of the chicken genome, and an abundance of single-nucleotide polymorphisms on the autosomes and sex chromosomes, will dramatically accelerate research on the molecular mechanisms of avian speciation over the next few years. The challenge for ornithologists is now to inform well studied examples of speciation in nature with increased molecular resolution-to clone speciation genes if they exist-and thereby evaluate the relative roles of extrinsic, intrinsic, deterministic, and stochastic causes for avian diversification.
Journal Article
Gene duplication and fragmentation in the zebra finch major histocompatibility complex
2010
Background
Due to its high polymorphism and importance for disease resistance, the major histocompatibility complex (MHC) has been an important focus of many vertebrate genome projects. Avian MHC organization is of particular interest because the chicken
Gallus gallus
, the avian species with the best characterized MHC, possesses a highly streamlined
minimal essential
MHC, which is linked to resistance against specific pathogens. It remains unclear the extent to which this organization describes the situation in other birds and whether it represents a derived or ancestral condition. The sequencing of the zebra finch
Taeniopygia guttata
genome, in combination with targeted bacterial artificial chromosome (BAC) sequencing, has allowed us to characterize an MHC from a highly divergent and diverse avian lineage, the passerines.
Results
The zebra finch MHC exhibits a complex structure and history involving gene duplication and fragmentation. The zebra finch MHC includes multiple Class I and Class II genes, some of which appear to be pseudogenes, and spans a much more extensive genomic region than the chicken MHC, as evidenced by the presence of MHC genes on each of seven BACs spanning 739 kb. Cytogenetic (FISH) evidence and the genome assembly itself place core MHC genes on as many as four chromosomes with TAP and Class I genes mapping to different chromosomes. MHC Class II regions are further characterized by high endogenous retroviral content. Lastly, we find strong evidence of selection acting on sites within passerine MHC Class I and Class II genes.
Conclusion
The zebra finch MHC differs markedly from that of the chicken, the only other bird species with a complete genome sequence. The apparent lack of synteny between
TAP
and the expressed MHC Class I locus is in fact reminiscent of a pattern seen in some mammalian lineages and may represent convergent evolution. Our analyses of the zebra finch MHC suggest a complex history involving chromosomal fission, gene duplication and translocation in the history of the MHC in birds, and highlight striking differences in MHC structure and organization among avian lineages.
Journal Article
A systems approach to animal communication
by
Hebets, Eileen A.
,
Mason, Paul H.
,
Balakrishnan, Christopher N.
in
Animal Communication
,
Animals
,
Degeneracy
2016
Why animal communication displays are so complex and how they have evolved are active foci of research with a long and rich history. Progress towards an evolutionary analysis of signal complexity, however, has been constrained by a lack of hypotheses to explain similarities and/or differences in signalling systems across taxa. To address this, we advocate incorporating a systems approach into studies of animal communication—an approach that includes comprehensive experimental designs and data collection in combination with the implementation of systems concepts and tools. A systems approach evaluates overall display architecture, including how components interact to alter function, and how function varies in different states of the system. We provide a brief overview of the current state of the field, including a focus on select studies that highlight the dynamic nature of animal signalling. We then introduce core concepts from systems biology (redundancy, degeneracy, pluripotentiality, and modularity) and discuss their relationships with system properties (e.g. robustness, flexibility, evolvability). We translate systems concepts into an animal communication framework and accentuate their utility through a case study. Finally, we demonstrate how consideration of the system-level organization of animal communication poses new practical research questions that will aid our understanding of how and why animal displays are so complex.
Journal Article