Rapid adaptation to novel environment

Steelhead (Oncorhynchus mykiss) are a migratory fish native to the northern Pacific Ocean and surrounding tributaries. In the native range, steelhead hatch in freshwater, migrate to the ocean to mature, and then return to freshwater to spawn. In the late 1890’s steelhead from California were intentionally introduced into Lake Michigan where they established naturally-reproducing populations. Steelhead in Lake Michigan continue to swim up rivers to spawn, but now treat the freshwater environment of the Great Lakes as a surrogate ocean. Along with my collaborators, I examined the genetic effects of the successful introduction and the effects of rapid adaptation to the novel Lake Michigan environment. To do so, we sequenced the genomes of 264 steelhead captured in the native and introduced ranges.

Location of steelhead sampling sites (A) and comparison of environmental conditions between native and introduced range (B). In total, 48 individuals were sampled from the Betsie and Little Manistee Rivers (in 1983-84) as well as Black and Platte Rivers (in 1998-99). Additionally, 24 individuals were sampled from the Betsie River in 1998-99 as well as Clear and Redwood Creeks. Sampling from the native range included anadromous individuals that are born in freshwater streams but then migrate to thePacific Ocean as juveniles while individuals sampled in Michigan are also born in freshwater streams but then use Lake Michigan as a surrogate ocean. Because the Pacific Ocean and Lake Michigan differ in salinity, the sampled steelhead populations were subject to vastly different salt and ion?transport processes in their respective environments (B).

 

 

 

 

 

 

 

 

 

 

 

 

 

 

Location of steelhead sampling sites (A) and comparison of environmental conditions between native and introduced range (B).Sampling from the native range included anadromous individuals that are born in freshwater streams but then migrate to the Pacific Ocean as juveniles while individuals sampled in Michigan are also born in freshwater streams but then use Lake Michigan as a surrogate ocean. Because the Pacific Ocean and Lake Michigan differ in salinity, the sampled steelhead populations were subject to vastly different salt and ion?transport processes in their respective environments (B).

Genome-wide heterozygosity

By comparing steelhead from Lake Michigan to steelhead from their ancestral population, we determined that the introduction led to a reduction in genome-wide levels of genetic diversity. This is important because reduction in genetic diversity may have resulted in reduced phenotypic variation available for selection to act.

Comparison of pooled heterozygosity across chromosomes and between populations. Mean heterozygosity, estimated for each 100 Kb window in 100 Kb steps, is illustrated by the solid line and the 95% confidence interval around each mean is illustrated with shading.

 

 

 

 

 

Comparison of pooled heterozygosity across chromosomes and between populations. Mean heterozygosity, estimated for each 100 Kb window in 100 Kb steps, is illustrated by the solid line and the 95% confidence interval around each mean is illustrated with shading.

Genomic signals of rapid adaptation

Despite this large reduction in genetic diversity, we also found three genomic regions strongly associated with rapid genetic adaptation to the novel environment. The first region altered the metabolic rates of steelhead in Lake Michigan compared to steelhead in the native Pacific population. This makes sense because we know that corals can modulate metabolic activity in response to environmental changes and we know that some species, such as cane toads, up-regulate metabolic genes at the range edge compared to the middle of the range.

SNPs and functions associated with a genomic region strongly linked to adaptation to the novel Lake Michigan environment. A) FST for all SNPs located within the outlier region, denoted by the extent of the black bracket, for both Pacific-Lake Michigan 1983-84 and Pacific-Lake Michigan 1998-99. Highlighted regions display the extent of the three genes located within the outlier region: 1) gram domain containing 4 (gramd4); 2) trichohyalin-like protein and 3) ceramide kinase (cerk). (B) For all SNPs where the minor allele frequency shifted by > 10%, allele frequency of the minor allele in all three populations. The gene gramd4 was marked by general drifting in the Lake Michigan population, which suggests relaxed natural selection in the introduced population. Conversely in cerk, selection across a larger range of minor allele frequencies resulted in near-fixation for all SNPs in 1983-84 Lake Michigan population. Although these effects were somewhat dampened by hatchery introgression that occurred after the early 1980s, this pattern reflects increased selection on cerk in the Lake Michigan populations. (C) When initiated by p73, GRAMD4 interacts with the mitochondria, initiating a chain of events that eventually results in cytochrome c release, caspase activation, and apoptosis. The CERK enzyme, however, phosphorylates ceramide forming C-1-P, which then activates DNA synthesis and cell division pathways.

 

The second and third regions contained genes that play a critical role in osmoregulation. Freshwater fish actively uptake ions from the environment to compensate for salts lost via passive diffusion while saltwater fish actively excrete ions to compensate for the passive diffusion of salts into their bodies. Anadromous salmonids can switch between these two processes, but this flexibility is both energetically costly and maladaptive for steelhead residing in an entirely freshwater environment. We found evidence of a large response to selection in Lake Michigan steelhead for two independent sets of genes, carbonic anhydrases and solute carriers, both of which facilitate uptake of ions from the aquatic environment. Additionally, blood pH changes have been observed after salinity alterations a result of a mismatch between carbonic anhydrase activity and ions needed to maintain pH. Thus, the increased ion-uptake in Lake Michigan steelhead not only maintains osmotic pressure, but also effectively regulates body pH in freshwater.

FST estimates for SNPs identified within regions associated with rapid adaptation. A and B) FST for all SNPs located within the outlier region, denoted by the extent of the black bracket, for both Pacific-Lake Michigan 1983-84 and Pacific-Lake Michigan 1998-99. Highlighted regions display the extent of the four genes located within the outlier regions: 1-3) carbonic anhydrases; 4) solute carrier family 26 member 6 (SLC26). Functionally, carbonic anhydrases break CO2 into H+ and HCO3-, which are then used to balance body pH. Similarly, SLC26 uptakes Cl- from the environment and releases cellular HCO3- into the environment (C). Both of these processes participate in osmoregulatory and acid-base balancing functions within the organism.

 

 

 

 

 

 

 

FST estimates for SNPs identified within regions associated with rapid adaptation. A and B) FST for all SNPs located within the outlier region, denoted by the extent of the black bracket, for both Pacific-Lake Michigan 1983-84 and Pacific-Lake Michigan 1998-99. Highlighted regions display the extent of the four genes located within the outlier regions: 1-3) carbonic anhydrases; 4) solute carrier family 26 member 6 (SLC26). Functionally, carbonic anhydrases break CO2 into H+ and HCO3, which are then used to balance body pH. Similarly, SLC26 uptakes Cl from the environment and releases cellular HCO3 into the environment (C). Both of these processes participate in osmoregulatory and acid-base balancing functions within the organism.