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

Abstract

Adaptive variation tends to emerge clinally along environmental gradients or discretely among habitats with limited connectivity. However, in Atlantic killifish (Fundulus heteroclitus), a population genetic discontinuity appears in the absence of obvious barriers to gene flow along parallel salinity clines and coincides with a physiologically stressful salinity. We show that populations resident on either side of this discontinuity differ in their abilities to compensate for osmotic shock and illustrate the physiological and functional genomic basis of population variation in hypoosmotic tolerance. A population native to a freshwater habitat, upstream of the genetic discontinuity, exhibits tolerance to extreme hypoosmotic challenge, whereas populations native to brackish or marine habitats downstream of the discontinuity lose osmotic homeostasis more severely and take longer to recover. Comparative transcriptomics reveals a core transcriptional response associated with acute and acclimatory responses to hypoosmotic shock and posits unique mechanisms that enable extreme osmotic tolerance. Of the genes that vary in expression among populations, those that are putatively involved in physiological acclimation are more likely to exhibit nonneutral patterns of divergence between freshwater and brackish populations. It is not the well-known effectors of osmotic acclimation, but rather the lesser-known immediateearly responses, that appear important in contributing to population differences.adaptive acclimation | ecological genomics | microarray A tlantic killifish (Fundulus heteroclitus) occupy an extremely wide osmotic niche from freshwater to marine, and populations are distributed along steep salinity gradients in Atlantic coast estuaries. In the Chesapeake Bay, salinity gradients are distributed across hundreds of kilometers, although no obvious barriers to gene flow exist across this continuum of osmotic habitats. Because salinity is arguably the most important single physical environmental variable that delimits aquatic species distributions in nature (including Fundulus species; ref. 1), we exploit F. heteroclitus distributed along Chesapeake Bay salinity gradients as a model to discover genes and pathways that enable extreme physiological plasticity and to explore the physiological and functional genomic basis of adaptive microevolution in alternative osmotic environments.Results and Discussion Population Genetic Divergence. We characterized the genetic structure of killifish distributed along two parallel salinity gradients in Chesapeake Bay: one along the Potomac River and the other along the James River (Fig. 1A). Steep clines in allele frequency for both mitochondrial and nuclear markers were centered at nearly identical salinities along the parallel gradients (Fig. 1B). Genotype frequency clines bounded the tidal freshwater transition region (<0.5 ppt) of both rivers, where sites upstream are freshwater year-round according to 20 y of data logged from fixed monitoring stations (www.chesapeakebay.net/ data_...

Steep, coincident, and concordant clines in mitochondrial and nuclear‐encoded genes in a hybrid zone between subspecies of Atlantic killifish,Fundulus heteroclitus

“…2004; Whitehead et al. 2011), and there are steep replicated clines in mtDNA and microsatellites in F. heteroclitus across salinity gradients in several large estuaries along the Atlantic coast, which is consistent with the action of environmental selection for freshwater tolerance in this species (Whitehead et al. 2011).…”

“…2011), and there are steep replicated clines in mtDNA and microsatellites in F. heteroclitus across salinity gradients in several large estuaries along the Atlantic coast, which is consistent with the action of environmental selection for freshwater tolerance in this species (Whitehead et al. 2011). Given this variation, it is possible that adult F. heteroclitus might prefer habitats of differing salinity for laying their eggs, which opens the possibility that assortative mating might be influencing genetic patterns at this locus.…”

Reciprocal osmotic challenges reveal mechanisms of divergence in phenotypic plasticity in the killifish Fundulus heteroclitus

“…A genetic discontinuity exists between geographically proximate populations along parallel salinity clines that transition between brackish and fresh waters of the eastern US despite no apparent barriers to gene flow. Freshwater populations show an increased capacity to acclimate to hypo-osmotic stress when compared with their brackish counterparts, consistent with adaptive divergence along this salinity gradient (Whitehead et al, 2011).…”

“…Since this osmotic compensatory response is energetically expensive (Kidder et al, 2006a,b), deterioration of the sensing, signaling and effector mechanisms that support this response may be expected under relaxed selection (Lahti et al, 2009). While F. heteroclitus populations derived from freshwater habitats, but reared in the laboratory in sea water, have a higher capacity for hypo-osmoregulation relative to populations from brackish and marine sites (Whitehead et al, 2011), their tolerance to hyper-saline water is unknown. In killifish, migration into freshwater habitats may be associated with relaxation of stabilizing selection that maintains the phenotypic plasticity necessary to tolerate salinity fluctuations typical of estuarine habitats.…”

Long prereproductive selection and divergence by depth in a Caribbean candelabrum coral

“…Such high connectivity is not uncommon to marine species with planktonic larval dispersal (4), ranging to extremes in which gene flow spans the broadest expanses of the Pacific Ocean (43). Thus, adaptive divergence occurs here despite the potential for high levels of gene flow (39). Such adaptive divergence under high gene flow generates a pattern where neutral genetic divergence is primarily partitioned by habitats, with little geographic structure.…”