Natural Selection Canalizes Expression Variation of Environmentally Induced Plasticity-Enabling Genes

Abstract

Many organisms survive fluctuating and extreme environmental conditions by manifesting multiple distinct phenotypes during adulthood by means of developmental processes that enable phenotypic plasticity. We report on the discovery of putative plasticity-enabling genes that are involved in transforming the gill of the euryhaline teleost fish, Fundulus heteroclitus, from its freshwater to its seawater gill-type, a process that alters both morphology and function. Gene expression that normally enables osmotic plasticity is inhibited by arsenic. Gene sets defined by antagonistic interactions between arsenic and salinity show reduced transcriptional variation among individual fish, suggesting unusually accurate and precise regulatory control of these genes, consistent with the hypothesis that they participate in a canalized developmental response. We observe that natural selection acts to preserve canalized gene expression in populations of killifish that are most tolerant to abrupt salinity change and that these populations show the least variability in their transcription of genes enabling plasticity of the gill. We found that genes participating in this highly canalized and conserved plasticity-enabling response had significantly fewer and less complex associations with transcriptional regulators than genes that respond only to arsenic or salinity. Collectively these findings, which are drawn from the relationships between environmental challenge, plasticity, and canalization among populations, suggest that the selective processes that facilitate phenotypic plasticity do so by targeting the regulatory networks that gives rise to the response. These findings also provide a generalized, conceptual framework of how genes might interact with the environment and evolve toward the development of plastic traits.

A novel variant of aquaporin 3 is expressed in killifish (Fundulus heteroclitus) intestine

“…Sequence analysis of the amplicons derived by RT-PCR of AQP3 identified a variant of kfAQP3 (kfAQP3a) in killifish gill that differed from our transcriptome database (kfAQP3b) in the three C-terminal amino acids (Jung et al, 2012a; Shaw et al, 2014). To examine the expression of these AQP3 variants in killifish intestine, intestines were isolated from nine fish acclimated to FW and nine fish acclimated to SW and stored in RNA later (Ambion, Austin, TX) at -20°C.…”

“…AQP3, AQP7, AQP9, and AQP10 have been identified in teleosts (Cerdà and Finn, 2010) and have been shown to play an important role in cellular arsenic uptake in zebrafish (Hamdi et al, 2009). The expression of kfAQP3 in the gill is salinity dependent reflecting its role in maintaining osmotic balance (Shaw et al, 2014; Whitehead et al, 2011). In a previous study we identified a novel AQP3 expressed in killifish gill (kfAQP3a), which is expressed in FW acclimated fish and does not transport arsenic (Jung et al, 2012a).…”

Considerations for the use of transcriptomics in identifying the ‘genes that matter’ for environmental adaptation

“…In populations able to acclimate to a wider range of environmental salinity, natural selection has targeted upstream regulators of transcription to more precisely control the expression of the downstream genes that enable phenotypic plasticity in response to salinity change. Consequently, gene networks in killifish populations that exhibit the broadest range of salinity tolerance have fewer transcriptional regulators and a more streamlined topology (Shaw et al, 2014). A meta-analysis of gene networks governing responses to the environment in bacteria that differ in their ability to tolerate a suite of abiotic factors also shows that most of the variation within environmentally regulated gene networks (in both gene sequence and gene content) occurs within upstream sensing and signal-transduction elements rather than downstream effector genes (Singh et al, 2008).…”

Genetic approaches in comparative and evolutionary physiology

“…As described above (Systems genetics), functional genomic analyses that are integrated with experimental analyses of physiological variation can provide the foundation and starting point for investigating the mechanistic and genetic basis of natural variation in whole animal performance (35,37,42,169,170,208,209).…”