The pace of the evolutionary change depends on the existence of genetic variation, population size and intensity of the selection. While environmental change very often exceeds the rate of evolution for many species, killifish (Fundulus heteroclitus), living in U.S Atlantic coast estuaries turn out to be remarkably resilient. They have adapted to survive levels of toxic industrial pollutants, tolerating concentrations up to 8000 times higher than sensitive fish. In this interesting study, Reid et al. use population genomic and transcriptomic analyses to reveal complex genetic basis of rapid adaptation in killifish to dramatic, human-induced, environmental change.
Four pairs of sensitive and tolerant populations were compared. Based on comparative trancriptomics and analysis of 384 whole genome sequences few candidate regions are identified to underlay tolerance to complex mixtures of polycyclic and halogenated aromatic hydrocarbons. Interestingly, they are shared among four tolerant populations and are highly ranked. This suggests that the most important targets of selection have evolved in parallel across polluted sites.
Within shared outliers are genes involved in aryl hydrocarbon receptor (AHR) signalling pathway. Role of this pathway is to mediate toxicity. Experiments showed that tolerant populations exhibit reduced inducibility of AHR regulated genes while sensitive populations showed up to 70 upregulated genes in response to pollutant. At the genetic level, the tolerant populations evolved in highly similar ways indicating constrained phenotypic variation. It seems that selection acts only on few genes.
Processes involved in the adaptation of killifish to lethal levels of environmental pollution are complex. AHR pathway is a key target of natural selection but potentially negative effects of its desensitisation lead to compensatory adaptations in genes responsible for estrogen and hypoxia signalling regulation of cell cycle or immune system function. Authors identified CYP1A dosage- compensating adaptation through gene duplications for impaired AHR signalling pathway. In northern tolerant populations CYP1A duplications have swept to high frequencies. Some individuals have up to eight copies of this gene. Other selective targets include genes outside AHR signalling pathway such as KCNB2 and KCNC3 genes whose products form conductance pore of the voltage-gated potassium channel. It seems to be very common that compensatory changes go along with rapid adaptive evolution.
This study underlies the role of high nucleotide diversity and extensive pre-existing genetic variation as crucial for selective sweeps and evolutionary rescue. Also, number of evolutionary solutions to this kind of pollution is limited. Even though this study showed that some species have the capacity to overcome severe environmental changes due to natural richness of their genetic pool, most of the species, unfortunately, are not able to adapt such rapid changes due to low level of genetic variation.
Reid, N. M., Proestou, D. A., Clark, B. W., Warren, W. C., Colbourne, J. K., Shaw, J. R., et al. (2016). The genomic landscape of rapid repeated evolutionary adaptation to toxic pollution in wild fish. Science (New York, N.Y.), 354(6317), 1305–1308.