The consequences of an introgression event

Abstract

The spread of adaptive alleles is fundamental to evolution, and in theory, this process is well-understood. However, only rarely can we follow this process-whether it originates from the spread of a new mutation, or by introgression from another population. In this issue of Molecular Ecology, Hanemaaijer et al. (2018) report on a 25-year long study of the mosquitoes Anopheles gambiae (Figure 1) and Anopheles coluzzi in Mali, based on genotypes at 15 single-nucleotide polymorphism (SNP). The species are usually reproductively isolated from each other, but in 2002 and 2006, bursts of hybridization were observed, when F1 hybrids became abundant. Alleles backcrossed from A. gambiae into A. coluzzi, but after the first event, these declined over the following years. In contrast, after 2006, an insecticide resistance allele that had established in A. gambiae spread into A. coluzzi, and rose to high frequency there, over 6 years (~75 generations). Whole genomesequences of 74 individuals showed that A. gambiae SNP from across the genome had become common in the A. coluzzi population, but that most of these were clustered in 34 genes around the resistance locus.A new set of SNP from 25 of these genes were assayed over time;over the 4 years since near-fixation of the resistance allele; some remained common, whereas others declined. What do these patterns tell us about this introgression event?In the absence of selection, when a single genome enters a population, most of it will be lost, but a few fragments may become common: the process of neutral introgression is highly random (Baird, Barton, & Etheridge, 2003). Here, there was a burst of hybridization, so that many genomes might have successfully entered A. coluzzi, reducing stochasticity. However, there must be strong net selection against introgression-the best evidence for this being that these two species have remained distinct, despite intermittent hybridization. The likely scenario is that despite this negative selection, one or more resistance alleles backcrossed into A. coluzzi, associated with some fragment of A. gambiae genome. Provided that the advantage of resistance outweighs the negative effects of the surrounding genome, this fragment will increase to high frequency. As it does so, the deleterious material will recombine away, producing smaller, and therefore fitter, introgressing blocks. In principle, the effective selection on the resistance allele will increase as fitter haplotypes outcompete the less fit. However, the process is highly random, and this pattern may be hard to detect. Thus, the selection coefficient of ~10% estimated by Hanemaaijer et al. (2018) is an approximate measure of the average effect of introgressing blocks on fitness, primarily due to the selective advantage of the resistance allele. Hanemaaijer et al. (2018) suggest that rates of decline of different SNP reflect selection on (or near) them: "the decrease in frequency of introgressed alleles proximal to the kdr mutation indicates that these alleles are maladaptive." However, ...

Eukaryote hybrid genomes

“…The effect of associative overdominance is strongest in low recombination regions, including inversions[78]. The balance between alleles and allelic combinations providing favourable phenotypic characters and the strength of selection against incompatibilities determine what introgression tracts will be inherited from which parent species upon hybridization (Fig 3)[21][79][80]. An insecticide resistance region was retained following a hybridization event in Anopheles coluzzi [21], suggesting a role for selection in maintaining favourable introgressed regions.…”

“…Evidence from altered expression patterns in synthetic hybrids and missing gene combinations in a hybrid species also suggest that DNA-repair[49][84][88] and genes involved in mutagenesis and cancer related pathways[84] may cause incompatibilities in hybrids. Genome formation in hybrid species is shaped by selection against incompatible combinations[43][73][79].…”

Comparing rates of introgression in parasitic feather lice with differing dispersal capabilities

“…Notably, recent studies have found that straggling and host-switching are relatively common processes in host-symbiont systems (De Vienne et al 2013;Bourguignon et al 2018;Nylin et al 2018;Doña et al 2019). Our study suggests that in a straggling/host-switching scenario, hybridization can provide further genetic variation with important ecological and evolutionary consequences (e.g., facilitating adaptation to current hosts or facilitating the colonization of new ones) (Barton 2018). Indeed, we may have found a potential recent hybridization event (i.e., the Physconelloides individual showing the highest level of introgression), though this requires further study to rule out methodological issues (e.g., wet-lab contamination).…”

Comparing rates of introgression in parasitic feather lice with differing dispersal capabilities

“…Notably, recent studies have found that straggling and host-switching are relatively common processes in host-symbiont systems [27][28][29][30] . Our study suggests that in a straggling/host-switching scenario, hybridization can provide further genetic variation with important ecological and evolutionary consequences (e.g., facilitating adaptation to current hosts or facilitating the colonization of new ones) 31 . Indeed, we may have found a potential recent hybridization event (i.e., the Physconelloides individual showing the highest level of introgression), though this requires further study to rule out methodological issues (e.g., wet-lab contamination).…”