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Cited by 118

The DOI matches its Crossref record; 47 of the 47 references it cites were found in a registry or an index.

Sexual and social stimuli elicit rapid and contrasting genomic responses

Cummings, Molly E, Larkins-Ford, Jonah, Reilly, Christian R.L, Wong, Ryan Y, Ramsey, Mary, Hofmann, Hans A·2008·Proceedings of the Royal Society B: Biological Sciences
DOI 10.1098/rspb.2007.1454PMC PMC2212751
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Abstract

Sensory physiology has been shown to influence female mate choice, yet little is known about the mechanisms within the brain that regulate this critical behaviour. Here we examine preference behaviour of 58 female swordtails, Xiphophorus nigrensis, in four different social environments (attractive and unattractive males, females only, non-attractive males only and asocial conditions) followed by neural gene expression profiling. We used a brain-specific cDNA microarray to identify patterns of genomic response and candidate genes, followed by quantitative PCR (qPCR) examination of gene expression with variation in behaviour. Our microarray results revealed patterns of genomic response differing more between classes of social stimuli than between presence versus absence of stimuli. We identified suites of genes showing diametrically opposed patterns of expression: genes that are turned ‘on’ while females interact with attractive males are turned ‘off’ when interacting with other females, and vice versa. Our qPCR results identified significant predictive relationships between five candidate genes and specific mate choice behaviours (preference and receptivity) across females exposed to males, with no significant patterns identified in female or asocial conditions or with overall locomotor activity. The identification of stimulus- and behaviour-specific responses opens an exciting window into the molecular pathways associated with social behaviour and mechanisms that underlie sexual selection.

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Crossref · 10.1098/rspb.2007.1454

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Figures

Figure 1 Female preference experimental tank. Stimuli (males LS or SS, females FF or nothing AA) are placed behind UV transparent plexiglas in the end zones of an experimental aquarium. Focal females are placed in the centre with three observational zones: 24 cm areas near each end zone (association zones) and a 24 cm ‘neutral’ zone in the centre. After a 5-min female acclimation period, female behaviour and association times are recorded for 15 min; stimuli are then switched and behaviour is recorded for another 15 min (to control for side biases).
Figure 1 Female preference experimental tank. Stimuli (males LS or SS, females FF or nothing AA) are placed behind UV transparent plexiglas in the end zones of an experimental aquarium. Focal females are placed in the centre with three observational zones: 24 cm areas near each end zone (association zones) and a 24 cm ‘neutral’ zone in the centre. After a 5-min female acclimation period, female behaviour and association times are recorded for 15 min; stimuli are then switched and behaviour is recorded for another 15 min (to control for side biases).CC BY · PubMed Central
Figure 2 Unsupervised hierarchical bootstrapped clustering of 306 significantly (PP≥0.99) differentially expressed genes across all four experimental conditions. Green represents significantly downregulated genes, red represents significantly upregulated genes and black represents intermediate levels of expression. Bootstrapping was used to obtain confidence values for the cluster nodes. Consensus trees were constructed by repeating the hierarchical clustering 1000 times on randomly permutated expression profiles using the hclust, consensus and heatmap functions in R/Bioconductor. A cluster node that emerges in every single iteration will be assigned a confidence value of 1.00, whereas a node that results from only half the iterations is assigned a value of 0.50.
Figure 2 Unsupervised hierarchical bootstrapped clustering of 306 significantly (PP≥0.99) differentially expressed genes across all four experimental conditions. Green represents significantly downregulated genes, red represents significantly upregulated genes and black represents intermediate levels of expression. Bootstrapping was used to obtain confidence values for the cluster nodes. Consensus trees were constructed by repeating the hierarchical clustering 1000 times on randomly permutated expression profiles using the hclust, consensus and heatmap functions in R/Bioconductor. A cluster node that emerges in every single iteration will be assigned a confidence value of 1.00, whereas a node that results from only half the iterations is assigned a value of 0.50.CC BY · PubMed Central
Figure 3 Mate choice and control-specific genes. The 128 genes (from figure 2) were significantly differentially expressed and predictive of specific social conditions (i.e. up- or downregulated in only one condition compared to all others; PP≥0.95). The y-axis indicates the number of unique genes significantly up- or downregulated in each environment with some genes identified to each group (complete list in table S1 in the electronic supplementary material). Red asterisk, neuroserpin precursor; blue asterisk, β1-adrenergic receptor.
Figure 3 Mate choice and control-specific genes. The 128 genes (from figure 2) were significantly differentially expressed and predictive of specific social conditions (i.e. up- or downregulated in only one condition compared to all others; PP≥0.95). The y-axis indicates the number of unique genes significantly up- or downregulated in each environment with some genes identified to each group (complete list in table S1 in the electronic supplementary material). Red asterisk, neuroserpin precursor; blue asterisk, β1-adrenergic receptor.CC BY · PubMed Central
Figure 4 Female locomotor (non-social) behaviour and egr-1 expression. Gene expression quantified by qPCR for 30 X. nigrensis females exposed to different social stimuli in experiment 2. Females exposed to the LS condition (large versus small male) are represented by dark blue squares; SS (two small males) by light blue squares, FF (two females) by green circles and AA (empty choice compartments) by red diamonds. Whole brain expression of egr-1 (×108) was normalized by Eavg CT/cDNA RiboGreen. Non-social locomotor activity is measured as the total number of transits through the centre (neutral zone) of the tank during the 30-min observation period (figure 1).
Figure 4 Female locomotor (non-social) behaviour and egr-1 expression. Gene expression quantified by qPCR for 30 X. nigrensis females exposed to different social stimuli in experiment 2. Females exposed to the LS condition (large versus small male) are represented by dark blue squares; SS (two small males) by light blue squares, FF (two females) by green circles and AA (empty choice compartments) by red diamonds. Whole brain expression of egr-1 (×108) was normalized by Eavg CT/cDNA RiboGreen. Non-social locomotor activity is measured as the total number of transits through the centre (neutral zone) of the tank during the 30-min observation period (figure 1).CC BY · PubMed Central
Figure 5 Female preference behaviour and gene expression in male exposure conditions. Gene expression quantified by qPCR for 30 X. nigrensis females exposed to different social stimuli in experiment 2 (LS and SS labels are the same as figure 4). Whole brain expression (normalized by Eavg CT/cDNA RiboGreen) for (a) neuroserpin precursor (×109), (b) neuroligin 3 (×109), (c) importin (×1010), (d) egr-1 (×108), (e) apyrase (×1012) and (f) β1-adrenergic receptor (×108). Preference scores are defined as proportion of association time with individual 1+log(1+glide displays towards individual 1/transits through centre of tank), where association time with individual 1 is greater than individual 2. Dashed lines indicate significant correlations at p<0.05. There were no significant correlations between preference behaviour and gene expression in female (FF) and asocial (AA) controls (table 1).
Figure 5 Female preference behaviour and gene expression in male exposure conditions. Gene expression quantified by qPCR for 30 X. nigrensis females exposed to different social stimuli in experiment 2 (LS and SS labels are the same as figure 4). Whole brain expression (normalized by Eavg CT/cDNA RiboGreen) for (a) neuroserpin precursor (×109), (b) neuroligin 3 (×109), (c) importin (×1010), (d) egr-1 (×108), (e) apyrase (×1012) and (f) β1-adrenergic receptor (×108). Preference scores are defined as proportion of association time with individual 1+log(1+glide displays towards individual 1/transits through centre of tank), where association time with individual 1 is greater than individual 2. Dashed lines indicate significant correlations at p<0.05. There were no significant correlations between preference behaviour and gene expression in female (FF) and asocial (AA) controls (table 1).CC BY · PubMed Central

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  1. Andersson M Sexual selection. 1994 Princeton NJ:Princeton University Press.

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Metadata

Authors
Cummings, M. E., Larkins-Ford, J., Reilly, C. R. L., Wong, R. Y., Ramsey, M., & Hofmann, H. A.
Affiliations
  • Section of Integrative Biology, University of TexasAustin, TX 78712, USA
  • Department of Biological Sciences, Hopkins Marine Station, Stanford UniversityPacific Grove, CA 93950, USA
Venue
Proceedings of the Royal Society B: Biological Sciences
Publisher
The Royal Society
Published
2007-12-05
Volume
275
Issue
1633
Pages
393-402
ISSN
  • 0962-8452
  • 1471-2954
DOI
10.1098/rspb.2007.1454
PMC
PMC2212751
Cited by
118
References
47
Language
en
Licence
royalsociety.org/journals/ethics-policies/data-sharing-mining/ (tdm)

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