Adaptive introgression enables evolutionary rescue from extreme environmental pollution

Abstract

Radical environmental change that provokes population decline can impose constraints on the sources of genetic variation that may enable evolutionary rescue. Adaptive toxicant resistance has rapidly evolved in Gulf killifish (Fundulus grandis) that occupy polluted habitats. We show that resistance scales with pollution level and negatively correlates with inducibility of aryl hydrocarbon receptor (AHR) signaling. Loci with the strongest signatures of recent selection harbor genes regulating AHR signaling. Two of these loci introgressed recently (18 to 34 generations ago) from Atlantic killifish (F. heteroclitus). One introgressed locus contains a deletion in AHR that confers a large adaptive advantage [selection coefficient (s) = 0.8]. Given the limited migration of killifish, recent adaptive introgression was likely mediated by human-assisted transport. We suggest that interspecies connectivity may be an important source of adaptive variation during extreme environmental change.

Contrasting signatures of introgression in North American box turtle (Terrapenespp.) contact zones

“…Furthermore, our data suggests a capacity for inter- and intraspecific adaptive introgression in this region. However, long term consequences are unknown – introgression may facilitate evolutionary rescue (Oziolor et al 2019), or drive extirpation either through genetic swamping of species or their merger (Todesco et al 2016). Also unknown are the levels of introgression that govern this relationship, as well as the demographic scenarios conducive to each.…”

Genetic signatures of evolutionary rescue by a selective sweep

“…Evolutionary rescue has been explored theoretically (e.g., Gomulkiewicz and Holt, 1995;Uecker and Hermisson, 2016;Anciaux et al, 2018) and observed repeatedly in both experiments (e.g., Bell and Gonzalez, 2009;Lindsey et al, 2013;Ramsayer et al, 2013) and in host-pathogen systems in nature (e.,g., Wei et al, 1995;Feder et al, 2016). More recently, a number of studies have used genetic data to suggest that evolutionary rescue has occurred in the wild, including crickets becoming song-less to avoid parasitoid flies (Pascoal et al, 2018, reviewed in McDermott, 2019, killifish deleting receptors to tolerate pollution (Oziolor et al, 2019), hares moulting brown instead of white to avoid predation in snowless winters (Jones et al, 2018), bats altering hibernation to survive white-nose syndrome (Gignoux-Wolfsohn et al, 2018), and tall waterhemp evolving herbicide resistance (Kreiner et al, 2019). In nearly all of these cases there is strong evidence of a recent selective sweep by a very beneficial allele.…”

“…In nearly all of these cases there is strong evidence of a recent selective sweep by a very beneficial allele. Genetic evidence for a demographic bottleneck, on the other hand, is generally lacking, although genome-wide reductions in nucleotide diversity and increases in Tajima's D, relative to non-stressed populations, are sometimes detected (Oziolor et al, 2019). This begs the question of whether one can infer evolutionary rescue from genetic data alone, which would greatly help in assessing the relevance of rescue in nature.…”

Genomic basis of parallel adaptation varies with divergence inArabidopsisand its relatives

“…1). Moreover, we found that allele reuse (repeated selection of the same haplotype, shared either via gene flow or from standing genetic variation) frequently underlies parallel adaptation between closely related lineages [29][30][31][32] , while parallelism from de-novo mutations dominates between distantly related taxa 13 . This suggests that the degree of allele reuse may be the primary mechanism behind the hypothesized divergence-dependency of parallel genome evolution, possibly reflecting either genetic (weak hybridization barriers, widespread ancestral polymorphism between closely related lineages 33 ) or ecological reasons (lower niche differentiation and geographical proximity 34,35 ).…”