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Reproduction Associated Gene Expression Under Predation Risk in Daphnia - a Comparative 2 Transcriptomic Approach

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Reproduction Associated Gene Expression Under Predation Risk in Daphnia - a Comparative 2 Transcriptomic Approach bioRxiv preprint doi: https://doi.org/10.1101/503904; this version posted December 25, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 Reproduction associated gene expression under predation risk in Daphnia - a comparative 2 transcriptomic approach 3 4 Verena Tams*1, Jana Helene Nickel*1, Anne Ehring1, Mathilde Cordellier1 5 6 7 * equal contribution 8 1 Universität Hamburg, Institut für Zoologie, Martin-Luther-King-Platz 3, 20146 Hamburg, 9 Germany 10 11 Corresponding author: [email protected], phone +49 (0)40-42838-3933 1 bioRxiv preprint doi: https://doi.org/10.1101/503904; this version posted December 25, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 12 Abstract 13 Organisms live in a dynamic and often challenging world. Phenotypic plastic responses allow 14 organisms to rapidly adjust to a new environmental situation. Although phenotypic plastic 15 responses to predation risk have been reported for the ecological and genomic model organism 16 Daphnia, their genetic basis is not well understood. Here, we characterized the transcriptional 17 profile of Daphnia galeata when exposed to fish kairomones. First, we investigated the 18 differential gene expression, identifying candidate transcripts being involved in shifts of life 19 history traits in D. galeata. A total of 125 differentially expressed transcripts (40 up- and 85 20 downregulated) were identified. The expression analysis revealed a surprisingly high variance 21 between clonal lines, likely reflecting their different life history strategies. Second, we applied a 22 gene co-expression network analysis to find clusters of tightly linked transcripts and reveal the 23 genetic pathways underlying predator-induced responses. Our results showed that transcripts 24 involved in remodeling of the cuticle, growth and digestion corresponded to life history shifts in 25 D. galeata. Furthermore, we compared our results with previous studies on other Daphnia 26 species to assess similarities in the predator-induced responses and Daphnia reproduction. 27 Orthologs were identified for D. magna related to predator-induced responses and for D. pulex 28 and D. galeata involved in reproduction. The unique combination of methods including the 29 comparative approach allowed for the identification of candidate transcripts, their functions 30 and orthologs associated with predator-induced responses and reproduction in Daphnia. 31 32 Keywords: RNA-seq, predator-induced response, gene co-expression, phenotypic plasticity, 33 Daphnia galeata 34 Introduction 35 Organisms are challenged throughout their lives by environmental changes that have an 36 impact on the health and fitness of each individual. Stress, an internal state initiated by an 37 external factor (stressor) is relative and has to be considered with respect to the ecological 38 niche of an individual (Van Straalen, 2003). A given phenotype that is advantageous in one 39 environmental setup might become disadvantageous in another. In general, organisms have 40 two possibilities to cope with environmental changes: return to the ecological niche by 41 behavioral (i.e. migration) or physiological changes, or change the boundaries of their 42 ecological niche by genetic adaptation (Van Straalen, 2003). The former is achieved at the 43 phenotypic level describing phenotypic plastic responses, while the latter is a genetic 2 bioRxiv preprint doi: https://doi.org/10.1101/503904; this version posted December 25, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 44 adaptation process, where genotypes with a higher fitness pass on their alleles to the next 45 generation. 46 Predation is an important biotic factor structuring whole communities (e.g., Aldana et 47 al., 2016; Boaden and Kingsford, 2015), maintaining species diversity (e.g., Estes et al., 2011; 48 Fine, 2015) and driving natural selection in populations (e.g., Kuchta and Svensson, 2014; 49 Morgans and Ord, 2013). Vertebrate as well as invertebrate aquatic predators, release 50 kairomones into the surrounding water (Macháček, 1991; Schoeppner and Relyea, 2009; Stibor, 51 1992; Stibor and Lüning, 1994). In some instances, kairomones can be detected by their prey, 52 inducing highly variable as well as predator-specific responses to reduce their vulnerability. 53 These predator-induced responses are a textbook example of phenotypic plasticity and have 54 been reported on in detail for a variety of Daphnia species (e.g., Boeing et al., 2006; Herzog et 55 al., 2016; Weider and Pijanowska, 1993; Yin et al., 2011). 56 57 Daphnia are small branchiopod crustaceans and are an isogenic model organism widely 58 used in ecology, evolution and ecotoxicology. Members of this family link trophic levels from 59 primary producers to consumers in freshwater ecosystems and are, therefore, vulnerable to 60 high predation risk (Lampert, 2011). Extensive shifts in behavior, morphology and life history 61 traits have been observed in response to predation and predation risk. The responses induced 62 by invertebrate predators include morphological changes such as the formation of helmets in D. 63 cucullata (e.g., Agrawal et al., 1999) and D. longispina (e.g., Brett, 1992) and the formation of 64 neck teeth in D. pulex (e.g., Tollrian, 1995). Vertebrate predators have been shown to induce 65 behavioral changes linked to diel vertical migration (DVM: an avoidance strategy; Cousyn et al., 66 2001; Effertz and Von Elert, 2017) as well as changes in life history traits (Boersma et al., 1998; 67 Effertz and Von Elert, 2017) in D. magna. The specificity of such predator-induced responses by 68 vertebrate and invertebrate kairomones has been shown, e.g. for the D. longispina species 69 complex from the Swiss lake Greifensee (Wolinska et al., 2007). The documented changes in life 70 history traits included a decrease in size at maturity when exposed to fish kairomones and an 71 increase when exposed to kairomones of the phantom midge larvae, a predatory invertebrate 72 of the genus Chaoborus. The species D. galeata is somehow peculiar since individuals exposed 73 to fish kairomones do not show a diel vertical migration behavior (Spaak and Boersma, 2001; 74 Stich and Lampert, 1981), nor do they produce morphological changes like helmets or neck 75 teeth (Tams et al., 2018). Long-term (14 days) exposure to fish kairomones in D. galeata 3 bioRxiv preprint doi: https://doi.org/10.1101/503904; this version posted December 25, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 76 revealed substantial life-historical variation within and among populations, as well as trends 77 congruent to previous studies such as a decrease in both age at first reproduction and somatic 78 growth rate in the presence of fish kairomones (Boersma et al., 1998; Stibor and Lüning, 1994; 79 Tams et al., 2018). 80 Although phenotypic plastic responses to predation risk have been extensively studied 81 in the ecological and genomic model organism Daphnia, their genetic basis is not well 82 understood. Combined approaches are necessary to understand the complexity of stress 83 responses, such as those induced by predators. Gene expression profiling and gene co- 84 expression analysis are current methods used to describe transcriptomes in different 85 organisms, e.g. plants (reviewed by Serin et al., 2016), vertebrates (Ghazalpour et al., 2006), 86 invertebrates (Zhao et al., 2016) and humans (reviewed by de la Fuente, 2010). Gene co- 87 expression network analysis is used to infer gene functions through the modular structure of 88 co-expressed genes and their functional relations (Bergmann et al., 2004). Genes within one co- 89 expression module often share conserved biological functions (Subramanian et al., 2005). 90 Hence, the transcriptional profile gains integrity when the modularity of the co-expressed 91 transcripts is taken into account, revealing potential genetic pathways. The co-expression 92 network of genes is constructed via an adjacency matrix (Langfelder and Horvath, 2008). 93 Modules, cluster of highly interconnected genes, are identified using hierarchical clustering 94 (Langfelder and Horvath, 2008). The benefit of the co-expression network analysis lies in the 95 opportunity to correlate gene expression and phenotype data (Langfelder and Horvath, 2008) 96 simplifying the process of candidate genes identification for further analysis or the design of 97 future experiments. 98 Fish is a predator of all species and common response patterns are found, while the 99 predator-induced responses mentioned above are known to vary across Daphnia species. One 100 can therefore expect that the genetic basis of these responses is conserved response across 101 species to a certain extent. Thus, a comparative transcriptomic approach will help reveal 102 common transcripts involved in predator-induced responses across Daphnia species. The 103 difficulty lies in finding homologous genes in species having diverged million years ago. 104 OrthoMCL is a tool used to identify clusters of orthologous genes (orthologs) that are 105 functionally conserved. The benefit of this tool is that known functions of orthologs in one 106 species can be inferred to assign putative functions to orthologs in another species (Li et al., 107 2003). The comparative transcriptomics approach made use of the existing OrthoMCL 108 information from the reference transcriptome of D.
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