Differential transcriptomic responses of ancient and modern Daphnia genotypes to phosphorus supply

Little is known about the role of transcriptomic changes in driving phenotypic evolution in natural populations, particularly in response to anthropogenic environmental change. Previous analyses of Daphnia genotypes separated by centuries of evolution in a lake using methods in resurrection ecology...

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Published inMolecular ecology Vol. 24; no. 1; pp. 123 - 135
Main Authors Roy Chowdhury, Priyanka, Frisch, Dagmar, Becker, Dörthe, Lopez, Jacqueline A., Weider, Lawrence J., Colbourne, John K., Jeyasingh, Punidan D.
Format Journal Article
LanguageEnglish
Published England Blackwell Publishing Ltd 01.01.2015
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Summary:Little is known about the role of transcriptomic changes in driving phenotypic evolution in natural populations, particularly in response to anthropogenic environmental change. Previous analyses of Daphnia genotypes separated by centuries of evolution in a lake using methods in resurrection ecology revealed striking genetic and phenotypic shifts that were highly correlated with anthropogenic environmental change, specifically phosphorus (P)‐driven nutrient enrichment (i.e. eutrophication). Here, we compared the transcriptomes of two ancient (~700‐year‐old) and two modern (~10‐year‐old) genotypes in historic (low P) and contemporary (high P) environmental conditions using microarrays. We found considerable transcriptomic variation between ‘ancient’ and ‘modern’ genotypes in both treatments, with stressful (low P) conditions eliciting differential expression (DE) of a larger number of genes. Further, more genes were DE between ‘ancient’ and ‘modern’ genotypes than within these groups. Expression patterns of individual genes differed greatly among genotypes, suggesting that different transcriptomic responses can result in similar phenotypes. While this confounded patterns between ‘ancient’ and ‘modern’ genotypes at the gene level, patterns were discernible at the functional level: annotation of DE genes revealed particular enrichment of genes involved in metabolic pathways in response to P‐treatments. Analyses of gene families suggested significant DE in pathways already known to be important in dealing with P‐limitation in Daphnia as well as in other organisms. Such observations on genotypes of a single natural population, separated by hundreds of years of evolution in contrasting environmental conditions before and during anthropogenic environmental changes, highlight the important role of transcriptional mechanisms in the evolutionary responses of populations.
Bibliography:NSF - No. 0924401; No. 1256867; No. 0924289; No. 1256881
Appendix S1 Fig. S1 Factorial design of Microarray experiment. Arrows indicate contrasts between (blue, direct comparisons) and within (red, indirect comparisons) ancient and modern populations respectively and numbers indicate replication. RNA was harvested from each treatment and competitively hybridized to the NimbleGen 12-plex long oligonucleotide microarray (for details see Lopez & Colbourne 2011). Table S1 Physiological data for "ancient" and "modern" temporal subpopulations in response to dietary P-supply (modified from Frisch et al. 2014). Phosphorus Use Efficiency (PUE) is the amount of biomass produced per unit of somatic P concentrations under P-limiting conditions. Data are means ± SD (n = 5). Growth rate (GR) is represented as the change in body length (top of the head to the base of the tail spine) in mm per day. Data are means ± SD (n = 10). Phosphorus kinetics in response to alterations in dietary P-supply in the four genotypes used in this study taken from previously published work. Retention Efficiency (RE) is the % of initial radioactivity (33P) retained in Daphnia after 12 h following 10 min of feeding on radioactive algae. Data are means ± SD (n = 3).Appendix S2 Enrichment of differentially expressed genes (FDR <0.05) in KEGG pathways. Numbers in the table indicate the enrichment score for pathways enriched by up-regulated genes (red), down-regulated genes (green) and those that were significantly enriched by both up- and down-regulated genes (yellow). In the latter case, both enrichment scores are shown. U=upregulated, D = downregulated. Pathways for Metabolism are shown in the Ipath maps of Fig. 2 of the main manuscript.Appendix S3 Enrichment of differentially expressed genes (FDR < 0.05) in different KOG categories. Daphnia pulex genes were assigned to KOG categories according to the Joint Genome Institute (http://genome.jgi-psf.org/cgi-bin/kogBrowser?db=Dappu1). For this analysis, only genes that could be assigned to a functional category were used. Statistical significance of enrichment was based on Fisher's exact test with multiple testing corrections using Bonferroni correction). 'O' (highlighted in yellow) and 'U' (highlighted in blue) indicate respectively over- and under representation of the different KOGs in the gene set in question (i.e., differentially expressed genes); 'n.s.' indicates functional groups/gene families with no significant enrichment in differentially expressed genes.Appendix S4 List of genes that were commonly differentially expressed in all four between-population contrasts (A vs. M genotypes) of the HiP and the LoP treatment. Note that only genes are shown that could be annotated to orthologous groups (KOG categories as defined by the Joint Genome Institute (http://genome.jgi-psf.org/cgi-bin/kogBrowser?db=Dappu1). Note that lineage-specific genes (83 genes in HiP and 91 genes in LoP), or those with annotations in other databases (KEGG, Enzyme commission (EC; Webb, '92), ARP2 database (see http://arthropods.eugenes.org/arthropods/), orthoDB7 on Arthropoda and Metazoa level (see http://orthodb.org/orthodb7) are not listed.
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ISSN:0962-1083
1365-294X
1365-294X
DOI:10.1111/mec.13009