Functional Genomics of Physiological Plasticity and Local Adaptation in Killifish

Abstract

Evolutionary solutions to the physiological challenges of life in highly variable habitats can span the continuum from evolution of a cosmopolitan plastic phenotype to the evolution of locally adapted phenotypes. Killifish (Fundulus sp.) have evolved both highly plastic and locally adapted phenotypes within different selective contexts, providing a comparative system in which to explore the genomic underpinnings of physiological plasticity and adaptive variation. Importantly, extensive variation exists among populations and species for tolerance to a variety of stressors, and we exploit this variation in comparative studies to yield insights into the genomic basis of evolved phenotypic variation. Notably, species of Fundulus occupy the continuum of osmotic habitats from freshwater to marine and populations within Fundulus heteroclitus span far greater variation in pollution tolerance than across all species of fish. Here, we explore how transcriptome regulation underpins extreme physiological plasticity on osmotic shock and how genomic and transcriptomic variation is associated with locally evolved pollution tolerance. We show that F. heteroclitus quickly acclimate to extreme osmotic shock by mounting a dramatic rapid transcriptomic response including an early crisis control phase followed by a tissue remodeling phase involving many regulatory pathways. We also show that convergent evolution of locally adapted pollution tolerance involves complex patterns of gene expression and genome sequence variation, which is confounded with body-weight dependence for some genes. Similarly, exploiting the natural phenotypic variation associated with other established and emerging model organisms is likely to greatly accelerate the pace of discovery of the genomic basis of phenotypic variation.

Salinity- and population-dependent genome regulatory response during osmotic acclimation in the killifish (Fundulus heteroclitus) gill

“…Previous studies have indicated that regulation of histone gene expression is associated with osmotic acclimation in killifish (Whitehead et al, 2011b;Whitehead et al, 2011a), and we detected several histone transcripts with transient upregulation in response to hypo-osmotic challenge (Fig.4E,F), two of which show salinitydependent upregulation (Fig.4E). Hypo-osmotic conditions can cause swelling of the nucleus and alter the structure and arrangement of chromatin, thereby potentially disrupting genome function (Finan and Guilak, 2010).…”

“…At each sampling time point, plasma was collected by caudal puncture and was immediately isolated for ion measurements, one gill basket was excised and preserved for electron microscopy, and the other gill basket was preserved in RNAlater (Ambion, Austin, TX, USA) for transcriptomics. This experimental procedure is directly comparable to that of previous studies (Whitehead et al, 2011a;Whitehead et al, 2011b). All fish were treated in accordance with approved institutional animal care and use protocols.…”

“…Samples were enclosed in a SureHyb microarray hybridization chamber (Agilent Technologies) and incubated at 60°C for 18h, following which slides were washed according to the manufacturer's protocols and scanned using a Packard BioScience Scanarray Express (PerkinElmer, Waltham, MA, USA), and images were processed using ImaGene (BioDiscovery, Inc., El Segundo, CA, USA). The microarray platform was the same as that used in Whitehead et al (Whitehead et al, 2011a;Whitehead et al, 2011b). Probes (N6800) were designed from F. heteroclitus expressed sequence tag (EST) sequences and included all ESTs that could be annotated.…”

Genomic mechanisms of evolved physiological plasticity in killifish distributed along an environmental salinity gradient

“…Gene expression was measured in gill tissues (the primary osmoregulatory tissue in fish; ref. 13) by using custom microarrays (14). Gene expression variation was characterized throughout the acclimation time-course and among populations, and patterns of population divergence were assigned to alternate evolutionary models: a putatively neutral model where population divergence in gene expression matches our isolationby-distance expectation ( Fig.…”

Host and Symbionts in Pocillopora damicornis Larvae Display Different Transcriptomic Responses to Ocean Acidification and Warming

“…Measurements of larval physiological condition, in this case, total protein, Symbiodinium density, and size, complement these transcriptomic data. Our exploration of responses to a changing environment at the level of the transcriptome yields valuable information about current physiological thresholds, mechanisms driving changes in biological processes, and the potential for physiological plasticity and tolerance (e.g., Hofmann et al, 2008;Todgham and Hofmann, 2009;Whitehead et al, 2010).…”