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Cited by 60

The DOI matches its Crossref record; 59 of the 59 references it cites were found in a registry or an index.

Behavior-dependent cis regulation reveals genes and pathways associated with bower building in cichlid fishes

York, Ryan A., Patil, Chinar, Abdilleh, Kawther, Johnson, Zachary V., Conte, Matthew A., Genner, Martin J., McGrath, Patrick T., Fraser, Hunter B., Fernald, Russell D., Streelman, J. Todd·2018·Proceedings of the National Academy of Sciences
DOI 10.1073/pnas.1810140115PMC PMC6255178
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Abstract

Significance: We do not fully understand how behavior evolves. Here we investigate the genomic basis of bower building among Lake Malawi cichlid fishes. Males construct bowers of two major types, pits and castles, to attract females in mating displays. Thousands of genetic variants are strongly associated with divergence in bower behavior. Remarkably, F 1 hybrids of pit-digging and castle-building species perform sequential construction of first pit and then castle bowers. Analysis of brain gene expression in hybrids showed behavior-dependent allele-specific expression with preferential expression of pit-digging alleles during pit digging and castle-building alleles during castle building. Our results suggest that behaviors evolve via complex genetic architectures featuring cis -regulatory differences whose effects on gene expression are specific and context dependent.

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Crossref · 10.1073/pnas.1810140115

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Figures

Fig. 1. Bower building. (A) Characteristic behavioral patterns associated with pit digging (Upper) and castle bower building (Lower). (B) Average locations of scoops (gray) and spits (red) during bower-building trials in the pit-digging species C. virginalis and the castle-building species M. conophoros. Consensus locations of the bowers are indicated by dashed black circles. (C) Results of a Student’s t test (two-tailed, P = 0.006) comparing difference score (in millimeters; mm) between C. virginalis (pit digging; yellow) and M. conophoros (castle building; green). (**P < 0.01.) (D) Maximum-likelihood phylogeny from genome-wide variants of the species sequenced in this study. Numbers at nodes are bootstrap support values.
Fig. 1. Bower building. (A) Characteristic behavioral patterns associated with pit digging (Upper) and castle bower building (Lower). (B) Average locations of scoops (gray) and spits (red) during bower-building trials in the pit-digging species C. virginalis and the castle-building species M. conophoros. Consensus locations of the bowers are indicated by dashed black circles. (C) Results of a Student’s t test (two-tailed, P = 0.006) comparing difference score (in millimeters; mm) between C. virginalis (pit digging; yellow) and M. conophoros (castle building; green). (**P < 0.01.) (D) Maximum-likelihood phylogeny from genome-wide variants of the species sequenced in this study. Numbers at nodes are bootstrap support values.CC BY-NC-ND · PubMed Central
Fig. 2. Genome-wide divergence associated with bower building. (A) Manhattan plot of genome-wide ZFST for SNPs and indels between pit-digging and castle-building species. (B) Semantic similarity of GO biological process terms enriched for high-FST variants. (C) Bar plot of SNP proportions per FST cutoff for ancestral and derived SNPs. SNPs in which castle-building species possess the alternate allele are colored red; those in which pit-digging species possess the alternate allele are colored blue. ***P < 0.001, Fisher’s exact test.
Fig. 2. Genome-wide divergence associated with bower building. (A) Manhattan plot of genome-wide ZFST for SNPs and indels between pit-digging and castle-building species. (B) Semantic similarity of GO biological process terms enriched for high-FST variants. (C) Bar plot of SNP proportions per FST cutoff for ancestral and derived SNPs. SNPs in which castle-building species possess the alternate allele are colored red; those in which pit-digging species possess the alternate allele are colored blue. ***P < 0.001, Fisher’s exact test.CC BY-NC-ND · PubMed Central
Fig. 3. Complex phylogenetic relationships among sand-dwelling Malawi cichlids. (A) We plotted 1,927 phylogenies resulting from nonoverlapping 10,000 SNP windows using DensiTree. The consensus phylogeny produced by DensiTree is colored black. (B) Bar plot of mean genome-wide weightings for the 15 tree topologies tested with Twisst. Trees grouping clades by bower phenotype (topologies 15, 10, and 3) are highlighted. See SI Appendix, Fig. S4 for visualizations of all 15 topologies. (C) An example of a stacked plot of topology weightings along a region of LG11 with strong support for groupings by phenotype. (D) An example of a stacked plot of a mixed-weight region on LG10. (E) Heatmap of the most significant f4 values. Species in the x and y axes were either B or C in the form f4(A,B;C, A. calliptera). Names of pit-digging and castle-building species are in blue and red font, respectively. A darker red square indicates more signal of gene flow between the species pairs in the respective row and column.
Fig. 3. Complex phylogenetic relationships among sand-dwelling Malawi cichlids. (A) We plotted 1,927 phylogenies resulting from nonoverlapping 10,000 SNP windows using DensiTree. The consensus phylogeny produced by DensiTree is colored black. (B) Bar plot of mean genome-wide weightings for the 15 tree topologies tested with Twisst. Trees grouping clades by bower phenotype (topologies 15, 10, and 3) are highlighted. See SI Appendix, Fig. S4 for visualizations of all 15 topologies. (C) An example of a stacked plot of topology weightings along a region of LG11 with strong support for groupings by phenotype. (D) An example of a stacked plot of a mixed-weight region on LG10. (E) Heatmap of the most significant f4 values. Species in the x and y axes were either B or C in the form f4(A,B;C, A. calliptera). Names of pit-digging and castle-building species are in blue and red font, respectively. A darker red square indicates more signal of gene flow between the species pairs in the respective row and column.CC BY-NC-ND · PubMed Central
Fig. 4. Behaviorally dependent allele-specific expression. (A) Cartoon representation of allele-specific expression under different contexts. In context 1, the sequence in the transcription factor binding site (TFBS1) is identical in the two alleles, leading to an expected ∼50:50 allelic ratio in the F1 hybrid. In context 2, there is a variant between the species in TFBS2 leading to ASE in the F1 hybrid. (B) Bar plots indicating the distribution of significantly differentially biased genes across building and digging contexts. Significance was calculated using a Fisher’s exact test; ***P < 5 × 10−5. (C) Semantic similarity of GO biological process terms enriched for genes with diffASE. Node size is the log of the size of the category represented. Nodes are colored by the log10 P value of the enrichment. (D) An example of a result from a sign test comparing context-dependent allele-specific expression (signal transduction; Reactome pathway R-HSA-162582).
Fig. 4. Behaviorally dependent allele-specific expression. (A) Cartoon representation of allele-specific expression under different contexts. In context 1, the sequence in the transcription factor binding site (TFBS1) is identical in the two alleles, leading to an expected ∼50:50 allelic ratio in the F1 hybrid. In context 2, there is a variant between the species in TFBS2 leading to ASE in the F1 hybrid. (B) Bar plots indicating the distribution of significantly differentially biased genes across building and digging contexts. Significance was calculated using a Fisher’s exact test; ***P < 5 × 10−5. (C) Semantic similarity of GO biological process terms enriched for genes with diffASE. Node size is the log of the size of the category represented. Nodes are colored by the log10 P value of the enrichment. (D) An example of a result from a sign test comparing context-dependent allele-specific expression (signal transduction; Reactome pathway R-HSA-162582).CC BY-NC-ND · PubMed Central
Fig. 5. Intersection of genome-wide SNPs and ASE. (A) Bar plot comparing the number of ASE, non-ASE, and diffASE (across all contexts) genes associated with highly divergent SNPs between pit-digging and castle-building species. ***P < 1 × 10−4, Fisher’s exact test comparing genes overlapping SNPs and genes not overlapping SNPs. (B) Categories in which the observed amount of overlap (blue) between genes associated with highly divergent SNPs and with ASE is significantly greater than expected (gray).
Fig. 5. Intersection of genome-wide SNPs and ASE. (A) Bar plot comparing the number of ASE, non-ASE, and diffASE (across all contexts) genes associated with highly divergent SNPs between pit-digging and castle-building species. ***P < 1 × 10−4, Fisher’s exact test comparing genes overlapping SNPs and genes not overlapping SNPs. (B) Categories in which the observed amount of overlap (blue) between genes associated with highly divergent SNPs and with ASE is significantly greater than expected (gray).CC BY-NC-ND · PubMed Central

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Research works printed but not linked: 1

  1. MHA Keenleyside Cichlid Fishes: Behavior, Ecology and Evolution (Chapman and Hall, 1st Ed, London, 1991).

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Metadata

Authors
York, R. A., Patil, C., Abdilleh, K., Johnson, Z. V., Conte, M. A., Genner, M. J., McGrath, P. T., Fraser, H. B., Fernald, R. D., & Streelman, J. T.
Affiliations
  • Department of Biology, Stanford University, Stanford, CA 94305;
  • School of Biological Sciences, Georgia Institute of Technology, Atlanta, GA 30332;
  • Department of Biology, University of Maryland, College Park, MD 20742;
  • School of Biological Sciences, University of Bristol, BS8 1TH Bristol, United Kingdom
ORCID
Patil, Chinar
Venue
Proceedings of the National Academy of Sciences
Publisher
National Academy of Sciences
Published
2018-11-05
Volume
115
Issue
47
ISSN
  • 0027-8424
  • 1091-6490
DOI
10.1073/pnas.1810140115
PMC
PMC6255178
Cited by
60
References
59
Language
en
Licence
creativecommons.org/licenses/by-nc-nd/4.0/ (vor)
Funders
  • HHS | National Institutes of Health (R01GM101095, 2R01GM097171-05A1, R21AG050304, R01GM114170)
  • HHS | NIH | National Institute of Neurological Disorders and Stroke (R01NINDS034950)

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