Cryptic genetic variation in brain gene expression precedes the evolution of cannibalism in spadefoot toad tadpoles
Data files
Apr 10, 2025 version files 317.27 MB
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CGV_Behavior.R
6.90 KB
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CGV_GE.R
68.13 KB
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README.md
15.98 KB
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sc_di_counts.gene.tsv
12.75 MB
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sc_diPhenoData_full.txt
4.79 KB
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sc_tel_counts.gene.tsv
12.69 MB
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sc_telPhenoData_full.txt
4.95 KB
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ScAg.txt
16.54 KB
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sp_di_counts.gene.tsv
4.34 MB
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sp_diPhenoData.txt
576 B
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sp_tel_counts.gene.tsv
4.34 MB
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sp_telPhenoData.txt
590 B
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survival.txt
37.89 KB
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trinotate_annotation_report.withToadNames.tsv
192.41 MB
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trinotate_annotation_report.withToadSymbols_Spea.tsv
90.59 MB
Abstract
The origins of novel behaviors are poorly understood, despite behavior’s hypothesized roles in evolution. One model, “genetic accommodation”, proposes that selection on ancestral phenotypic plasticity may precede the evolution of novel traits. A critical assumption of genetic accommodation is that ancestral lineages possess heritable genetic variation for trait plasticity that is revealed in novel environments, thereby providing the raw materials for subsequent refinement of the novel trait in derived lineages. Here, we use a combination of behavioral and RNA-seq approaches to test this assumption in the context of a novel tadpole behavior: predatory cannibalism. Cannibalism evolved in the spadefoot genus Spea, where an invertebrate diet induces a carnivorous tadpole morph capable of consuming live conspecific tadpoles. In contrast, closely related Scaphiopus tadpoles do not induce this carnivorous phenotype. Through species comparisons, we found that ancestral Spea likely expressed behavioral plasticity and harbored latent (i.e., “cryptic”) genetic variation in brain gene expression plasticity associated with cannibalism-inducing cues. Further, we found this cryptic genetic variation contains genes specifically associated with a dietary response and cannibalism in derived Spea. Our results suggest that novel behaviors, alongside novel morphologies, can evolve via the process of genetic accommodation. More generally, our results provide key evidence for the plausibility of genetic accommodation, revealing for the first time that cryptic genetic variation — the raw material for the evolution of novel traits — exists in natural populations at the level of gene expression.
This readme file was generated on 2024-02-24 by Dante J. Nesta
GENERAL INFORMATION
Title of Dataset: Cryptic genetic variation in brain gene expression precedes the evolution of cannibalism in spadefoot toad tadpoles
1st Author/Corresponding Author Information
Name: Dante J. Nesta
ORCID: 0009-0007-8206-660X
Institution: Indiana University Bloomington
Address: 915 E 3rd St, Bloomington, IN 47405
Institutional Email: dnesta@iu.edu
Alternative Email: dantenesta1@gmail.com
2nd Author/Principal Investigator Information
Name: Cristina C. Ledón-Rettig
ORCID: 0000-0002-1417-7486
Institution: Indiana University Bloomington
Address: 915 E 3rd St, Bloomington, IN 47405
Email: crisledo@iu.edu
Date of data (animal) collection: 2022-04-25
Geographic location of data collection: 38°59’40.3”N, 87°01’04.9”W
Information about funding sources that supported the collection of the data: NSF grant DEB-1754136
DATA & FILE OVERVIEW
File List:
ScAg.txt - Trait/behavior data for Scaphiopus holbrookii samples
survival.txt - Survival data for Scaphiopus holbrookii samples
trinotate_annotation_report.withToadNames.tsv - Annotated transcriptome of Scaphiopus holbrookii
trinotate_annotation_report.withToadSymbols_Spea.tsv - Annotated transcriptome of Spea bombifrons
sc_di_counts.gene.tsv - RNA-seq raw counts of Scaphiopus holbrookii diencephalon tissue
sc_tel_counts.gene.tsv - RNA-seq raw counts of Scaphiopus holbrookii telencephalon tissue
sp_di_counts.gene.tsv - RNA-seq raw counts of Spea bombifrons diencephalon tissue
sp_tel_counts.gene.tsv - RNA-seq raw counts of Spea bombifrons telencephalon tissue
sc_diPhenoData_full.txt - Treatment/phenotype data for Scaphiopus holbrookii samples (for diencephalon tissue)
sc_telPhenoData_full.txt - Treatment/phenotype data for Scaphiopus holbrookii samples (for diencephalon tissue)
sp_diPhenoData.txt - Treatment/phenotype data for Spea bombifrons samples (for diencephalon tissue)
sp_telPhenoData.txt - Treatment/phenotype data for Spea bombifrons samples (for telencephalon tissue)
CGV_Behavior.R - R script to run trait and behavioral analyses
CGV_GE.R - R script to run gene expression analyses
Relationship between files, if important:
“ScAg.txt” and “survival.txt” are to be used with “CGV_Behavior.R”
“trinotate_annotation_report.withToadNames.tsv”, “trinotate_annotation_report.withToadSymbols_Spea.tsv”, “sc_di_counts.gene.tsv”, “sc_tel_counts.gene.tsv”, “sp_di_counts.gene.tsv”, “sp_tel_counts.gene.tsv”, “sc_diPhenoData_full.txt”, “sc_telPhenoData_full.txt”, “sp_diPhenoData.txt”, and “sp_telPhenoData.txt” are to be used with “CGV_GE.R”
Additional related data collected that was not included in the current data package: N/A
METHODOLOGICAL INFORMATION
Description of methods used for collection/generation of data: See manuscript.
Methods for processing the data: See manuscript.
Software-specific information needed to interpret the data:
R (v4.2.2)
RStudio (v2022.12.0+353)
BiocManager (v1.30.22)
car (v3.1-2)
DESeq2 (v1.38.3)
edgeR (v3.40.2)
glmmTMB (v1.1.9)
lme4 (v1.1-35.1)
lmerTest (v3.1-3)
lmtest (v0.9-40)
PCAtest (v0.0.2)
RColorBrewer (v1.1-3)
survival (v3.5-8)
survminer (v0.4.9)
tidyverse (v2.0.0)
variancePartition (v1.28.9)
Standards and calibration information, if appropriate: N/A
Environmental/experimental conditions:
Diet - Food items that individuals in experiment were exclusively fed during early life (e.g., detritus or brine shrimp).
Density - Conspecific density that individuals in experiment experienced within rearing containers during early life (e.g., 3 individuals or 8 individuals).
Family - Sibship that individuals belonged to, determined by which egg clutches they hatched from.
Cannibalism - Quantification of how many individuals disappeared from each rearing container overnight across the experiment.
Describe any quality-assurance procedures performed on the data: N/A
People involved with sample collection, processing, analysis and/or submission:
Nathan J. Engbrecht - Locating ephemeral pools with Sc. holbrookii present
Sarah R. Lagon - Collecting eggs and help rearing animals
Katie M. Lo - Help rearing animals
Brandon Olson - Gosner staging samples
Daniel L. Woods - Quantifying behaviors
Aaron M. Buechlein - Sequencing, transcriptome assembly, QC of expression data, preliminary interpretation of data
Ram Podicheti - QC of expression data, interpretation of data
Douglas Rusch - Sequencing, transcriptome assembly, QC of expression data, interpretation of data
Alex Shepard - Manuscript feedback
C. Hal Terry - Manuscript feedback
Eleanor Shell - Manuscript feedback
Erica Nadolski - Manuscript feedback
DATA-SPECIFIC INFORMATION FOR: ScAg.txt
Number of variables: 21
Number of cases/rows: 256
Variable List:
ID - Sample identification number.
Family - Sibship that each sample belonged to.
Diet - Food items that animals were fed throughout the experiment; either shrimp or detritus.
Density - Conspecific density that animals were subjected to during the experiment; either high (8 animals per container) or low (3 animals per container).
Day_0 - Number of live animals counted in each container after placement into treatments.
Day_1 - Number of live animals counted in each container on day 1.
Day_2 - Number of live animals counted in each container on day 2.
Day_3 - Number of live animals counted in each container on day 3.
Day_4 - Number of live animals counted in each container on day 4.
Day_5 - Number of live animals counted in each container on day 5.
Day_6 - Number of live animals counted in each container on day 6.
Day_7 - Number of live animals counted in each container on day 7.
Cannibalism - Cumulative number of animals that disappeared per container over the course of 8 days.
X24h_cannibalism - After behavioral assays, animals were kept unfed alongside their stimulus animal for 24 hours before being fed prior to sacrifice and dissection. This variable describes whether the focal animal consumed their paired stimulus animal during this 24-hour period.
Dissection_day - Indicates the date that animal was sacrificed and dissected.
Gosner_stage - Indicates the stage of development of each individual following dissection.
Mass - Indicates the mass (in grams) of each individual prior to dissection.
Visibility - Indicates (in %) frames in the animal was successfully tracked by ToxTrac (animal tracking software) throughout recorded behavior assays.
Ave_speed - Mean average speed of each animal during behavioral assays (in mm/s).
Ave_acceleration - Mean average acceleration of each animal during behavioral assays (in mm/s^2).
Tot_dist - Total distance traveled by each animal during behavioral assays (in mm).
Missing data codes: Missing data represented by NAs and blank cells.
Specialized formats or other abbreviations used: N/A
DATA-SPECIFIC INFORMATION FOR: survival.txt
Number of variables: 7
Number of cases/rows: 1318
Variable List:
ID - Sample identification number.
Microcosm - Container that each animal was reared in.
Family - Sibship that each sample belonged to.
Diet - Food items that animals were fed throughout the experiment; either shrimp or detritus.
Density - Conspecific density that animals were subjected to during the experiment; either high (8 animals per container) or low (3 animals per container).
Time1 - Day (out of 8) that each animal was last recorded alive.
Status1 - Alive/dead status of each individual; 1 means animal survived, 0 means they did not.
Missing data codes: None
Specialized formats or other abbreviations used: N/A
DATA-SPECIFIC INFORMATION FOR: trinotate_annotation_report.withToadNames.tsv
Number of variables: 20
Number of cases/rows: 95118
Variable List:
Gene_id - Gene identifier.
Transcript_id - Transcript identifier.
Sprot_Top_BLASTX_hit - SwissProt BLASTX hit accession number.
RNAMMER - Predicted rRNAs.
Prot_id - Protein identifier.
Prot_coords - Mapped coordinates of amino acid sequence to DNA sequence.
Sprot_Top_BLASTP_hit - SwissProt BLASTP hit accession number.
Xenopus_proteome_BLASTX - BLASTX match to Xenopus tropicalis proteome.
Spea_multiplicata_proteome_BLASTX - BLASTX match to Spea multiplicata proteome.
Pfam - Pfam database protein family hits.
SignalP - Predicted signal peptides.
TmHMM - Predicted transmembrane proteins.
Eggnog - EggNOG orthology annotation.
Kegg - KEGG orthology annotation.
Gene_ontology_BLASTP - Gene ontology results of BLASTP hits.
Gene_ontology_Pfam - Gene ontology results of protein family hits.
Xenopus_Gene_Symbol - Xenopus laevis gene symbol.
Xenopus_Gene_Description - Xenopus laevis gene description.
Spea_multiplicata_GeneSymbol - Spea multiplicata gene symbol.
Missing data codes: Missing data represented by periods (.)
DATA-SPECIFIC INFORMATION FOR: trinotate_annotation_report.withToadSymbols_Spea.tsv
Number of variables: 20
Number of cases/rows: 96139
Variable List:
X.gene_id - Gene identifier.
Transcript_id - Transcript identifier.
Sprot_Top_BLASTX_hit - SwissProt BLASTX hit accession number.
RNAMMER - Predicted rRNAs.
Prot_id - Protein identifier.
Prot_coords - Mapped coordinates of amino acid sequence to DNA sequence.
Sprot_Top_BLASTP_hit - SwissProt BLASTP hit accession number.
Xenopus_proteome_BLASTX - BLASTX match to Xenopus tropicalis proteome.
Spea_multiplicata_proteome_BLASTX - BLASTX match to Spea multiplicata proteome.
Pfam - Pfam database protein family hits.
SignalP - Predicted signal peptides.
TmHMM - Predicted transmembrane proteins.
Eggnog - EggNOG orthology annotation.
Kegg - KEGG orthology annotation.
Gene_ontology_BLASTX - Gene ontology results of BLASTX hits.
Gene_ontology_BLASTP - Gene ontology results of BLASTP hits.
Gene_ontology_Pfam - Gene ontology results of protein family hits.
Xenopus_Gene_Symbol - Xenopus laevis gene symbol.
Xenopus_Gene_Description - Xenopus laevis gene description.
Spea_multiplicata_GeneSymbol - Spea multiplicata gene symbol.
Missing data codes: Missing data represented by periods (.)
DATA-SPECIFIC INFORMATION FOR: sc_di_counts.gene.tsv
Number of variables: 91
Number of cases/rows: 37660
Variable List:
TranscriptID - Transcript identifier.
XenopusBlastHit - Xenopus laevis BLASTN hit accession number.
XenopusGeneSymbol - Xenopus laevis gene symbol.
XenopusDescription - Xenopus laevis gene description.
Spea_multiplicata_BlastHit - Spea multiplicata BLASTN hit accession number.
Spea_multiplicataGeneName - Spea multiplicata gene name.
SwissProtBlastAccession - SwissProt homology search hit accession number.
SwissProtBlastHitTitle - SwissProt homology search hit identifier.
Variables 9-91 - Sample identification numbers of Scaphiopus holbrookii diencephalon tissues.
Missing data codes: Missing data represented by periods (.)
DATA-SPECIFIC INFORMATION FOR: sc_tel_counts.gene.tsv
Number of variables: 91
Number of cases/rows: 37660
Variable List:
TranscriptID - Transcript identifier.
XenopusBlastHit - Xenopus laevis BLASTN hit accession number.
XenopusGeneSymbol - Xenopus laevis gene symbol.
XenopusDescription - Xenopus laevis gene description.
Spea_multiplicata_BlastHit - Spea multiplicata BLASTN hit accession number.
Spea_multiplicataGeneName - Spea multiplicata gene name.
SwissProtBlastAccession - SwissProt homology search hit accession number.
SwissProtBlastHitTitle - SwissProt homology search hit identifier.
Variables 9-91 - Sample identification numbers of Scaphiopus holbrookii telencephalon tissues.
Missing data codes: Missing data represented by periods (.)
DATA-SPECIFIC INFORMATION FOR: sp_di_counts.gene.tsv
Number of variables: 15
Number of cases/rows: 76784
Variable List:
TranscriptID - Transcript identifier.
Variables 2-15 - Sample identification numbers of Spea bombifrons diencephalon tissues.
Missing data codes: Missing data represented by periods (.)
DATA-SPECIFIC INFORMATION FOR: sp_tel_counts.gene.tsv
Number of variables: 15
Number of cases/rows: 76784
Variable List:
TranscriptID - Transcript identifier.
Variables 2-15 - Sample identification numbers of Spea bombifrons telencephalon tissues.
Missing data codes: Missing data represented by periods (.)
DATA-SPECIFIC INFORMATION FOR: sc_diPhenoData_full.txt
Number of variables: 8
Number of cases/rows: 83
Variable List:
Sample - Complete sample identifier (Sample number, tissue, and species).
Food - Food items that animals were fed throughout the experiment; either shrimp or detritus. Synonymous with ‘Diet’ in other datasets.
Density - Conspecific density that animals were subjected to during the experiment; either high (8 animals per container) or low (3 animals per container).
Family - Sibship that each sample belonged to.
Cannibalism - Cumulative number of animals that disappeared per container over the course of 8 days.
Gosner_stage - Indicates the stage of development of each individual following dissection.
Region - Brain region information (All diencephalon).
ID - Sample identification number.
Missing data codes: Missing data represented by blank cells
DATA-SPECIFIC INFORMATION FOR: sc_telPhenoData_full.txt
Number of variables: 8
Number of cases/rows: 83
Variable List:
Sample - Complete sample identifier (Sample number, tissue, and species).
Food - Food items that animals were fed throughout the experiment; either shrimp or detritus. Synonymous with ‘Diet’ in other datasets.
Density - Conspecific density that animals were subjected to during the experiment; either high (8 animals per container) or low (3 animals per container).
Family - Sibship that each sample belonged to.
Cannibalism - Cumulative number of animals that disappeared per container over the course of 8 days.
Gosner_stage - Indicates the stage of development of each individual following dissection.
Region - Brain region information (All telencephalon).
ID - Sample identification number.
Missing data codes: Missing data represented by blank cells
DATA-SPECIFIC INFORMATION FOR: sp_diPhenoData.txt
Number of variables: 4
Number of cases/rows: 14
Variable List:
Sample - Complete sample identifier (Sample number, tissue, and species).
Food - Food items that animals were fed throughout the experiment; either shrimp or detritus. Synonymous with ‘Diet’ in other datasets.
Density - Conspecific density that animals were subjected to during the experiment; either high (8 animals per container) or low (3 animals per container).
Morph - Resulting ecomorph induced by treatment conditions following conclusion of the experiment (Either omnivore morph or carnivore morph).
Missing data codes: None
DATA-SPECIFIC INFORMATION FOR: sp_telPhenoData.txt
Number of variables: 4
Number of cases/rows: 14
Variable List:
Sample - Complete sample identifier (Sample number, tissue, and species).
Food - Food items that animals were fed throughout the experiment; either shrimp or detritus. Synonymous with ‘Diet’ in other datasets.
Density - Conspecific density that animals were subjected to during the experiment; either high (8 animals per container) or low (3 animals per container).
Morph - Resulting ecomorph induced by treatment conditions following conclusion of the experiment (Either omnivore morph or carnivore morph).
Missing data codes: None
SHARING/ACCESS INFORMATION
Licenses/restrictions placed on the data: N/A
Links to publications that cite or use the data: TBD
Links to other publicly accessible locations of the data: N/A
Links/relationships to ancillary data sets: N/A
Was data derived from another source?
If yes, list source(s): No
Recommended citation for this dataset: D. J. Nesta, C. C. Ledón-Rettig, Data from “Cryptic genetic variation in brain gene expression precedes the evolution of cannibalism in spadefoot toad tadpoles.” Dryad. Available at 10.5061/dryad.ncjsxkt6n.