Humans are altering Earth’s systems to such an extent that the geological period in which we are living has been dubbed the Anthropocene (1). Climate change, human land use, and the chemicals used in everyday living challenge biological species by creating new environments to which they must rapidly adapt or go extinct (1, 2). Can species evolve fast enough to survive? On page 455 of this issue, Oziolor et al. (3) show that the answer can be yes. The authors report that a fish species rapidly adapted to toxins in a highly polluted region of the Gulf of Mexico. They identify gene exchange between species by hybridization (introgression) as the mechanism enabling rapid adaptation and rescue of populations that might have otherwise gone extinct.
Traditionally, scientists have considered adaptive evolution to be a slow process. Yet, an increasing number of studies have shown that species can adapt rapidly to environmental challenges (2). Such rapid adaptation provides hope that species can adapt to the profound changes occurring in our human-dominated world. Failure to adapt means that species go locally, and possibly globally, extinct. The challenge for biologists is to explain why some species rapidly adapt when others fail. The stakes for solving this challenge are high: Humans are inducing one of Earth’s mass extinction events (4), and a better understanding of when and how species adapt to environmental stressors can provide critical information for conservation efforts.
A key determinant of adaptive potential is how much genetic variation a population harbors. When such variation is present, populations confronted with environmental change can potentially respond through rapid evolutionary change. Without genetic variation, a population cannot evolve. The problem is that, when populations experience environmental challenges, population size declines because individuals die or fail to reproduce. And when populations lose individuals, they lose variation too. The result is a negative feedback loop. The more individuals die or fail to reproduce, the less likely it becomes that a population can adapt; the less adapted a population, the more individuals die or don’t reproduce. Breaking out of this feedback loop requires an influx of new genetic variation. Populations typically acquire this new variation through mutation or gene flow from other populations. Yet, adaptive mutations might not arise quickly enough to rescue declining populations before they go extinct, and gene flow from other populations often brings in variation that is only adaptive in the population’s old environment, not the new one (4).
Oziolor et al. show that Gulf killifish rapidly adapted to toxins in a polluted region of the Gulf of Mexico after mating with a related fish species, Atlantic killifish. This hybridization resulted in the exchange of adaptive genes that are involved in toxin resistance.
GRAPHIC: V. ALTOUNIAN/SCIENCE
Hybridization between species is a crucial source of genetic variation that can fuel adaptation to new environments (5–7). But hybridization can also be an evolutionary dead end and a threat to diversity; it can reduce population fitness and cause species to collapse. Given that new species are increasingly introduced into many habitats through trade and other human activities, hybridization’s role as a creative force, as opposed to a destructive one, is a controversial issue of pressing importance (8, 9).
Oziolor et al. address this problem by asking whether hybridization has rescued declining populations of Gulf killifish (Fundulus grandis) by facilitating rapid adaptation to a new human threat. Using population surveys and experimental measures of toxic resistance, they show that Gulf killifish from polluted areas in Galveston Bay, USA, are resistant to toxins that cause lethal heart deformities. Using genomic analyses, the authors further show that populations in the most polluted areas were less genetically diverse than those in the less polluted habitat, as is expected if Gulf killifish population declined because of pollution (see the figure).
Oziolor et al. also report evidence of natural selection on genomic regions that include genes involved in the observed toxic resistance. The source of the adaptive genetic variation at these loci is a different species: the Atlantic killifish (Fundulus heteroclitus). The Gulf killifish appear to have acquired these genetic variants by mating (hybridizing) with the Atlantic killifish.
It is unclear why Atlantic killifish harbor genetic variation that is adaptive in Gulf killifish experiencing pollution. This touches on a more general question regarding adaptive introgression: Is such variation favored by natural selection in the donor species? If so, hybridization might enable species to capture adaptive variants from other species that have already undergone the adaptive process. Alternatively, genetic variation derived from the donor species might only be adaptive in the recipient species, depending on how that variation interacts with the rest of the recipient species’ genome and environment. If this is so, it might be more difficult to predict under which conditions introgression will be adaptive.
Regardless of these considerations, Oziolor et al.‘s results provide compelling evidence of evolutionary rescue of a declining population through hybridization. Ironically, humans might have provided the opportunity for such rescue. Whereas Gulf killifish are found in the Gulf of Mexico, Atlantic killifish are normally found along the Atlantic coast of North America, outside of the geographic region where the Gulf killifish occur. Oziolor et al. suggest that the Atlantic killifish might have been transported by humans into Galveston Bay through discharge of ship ballast water. Thus, introduction of this species into Gulf killifish habitat by humans might have enabled hybridization—and therefore evolutionary rescue—to occur.
The process of adaptive introgression observed by Oziolor et al. is not specific to extreme situations of human-introduced species or human-impacted environments. Genomic studies have revealed that hybridization is more common than expected in many species and that it might have fueled bursts of adaptive diversification throughout Earth’s evolutionary history (6, 7, 10). But despite its potential to contribute to diversity, hybridization carries risks and can even threaten species with extinction (8, 9). To guide conservation efforts, scientists need to clarify the conditions under which hybridization diminishes rather than enhances biodiversity in a rapidly changing world.
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