Genomic Admixture Analysis in European Populus spp. Reveals Unexpected Patterns of Reproductive Isolation and Mating

Abstract

Admixture between genetically divergent populations facilitates genomic studies of the mechanisms involved in adaptation, reproductive isolation, and speciation, including mapping of the loci involved in these phenomena. Little is known about how pre-and postzygotic barriers will affect the prospects of ''admixture mapping'' in wild species. We have studied 93 mapped genetic markers (microsatellites, indels, and sequence polymorphisms, $60,000 data points) to address this topic in hybrid zones of Populus alba and P. tremula, two widespread, ecologically important forest trees. Using genotype and linkage information and recently developed analytical tools we show that (1) reproductive isolation between these species is much stronger than previously assumed but this cannot prevent the introgression of neutral or advantageous alleles, (2) unexpected genotypic gaps exist between recombinant hybrids and their parental taxa, (3) these conspicuous genotypic patterns are due to assortative mating and strong postzygotic barriers, rather than recent population history. We discuss possible evolutionary trajectories of hybrid lineages between these species and outline strategies for admixture mapping in hybrid zones between highly divergent populations. Datasets such as this one are still rare in studies of natural hybrid zones but should soon become more common as high throughput genotyping and resequencing become feasible in nonmodel species.

Hybridization in contact zone between temperate European pine species

“…This approach has recently been developed in several model plant species demonstrating the role of hybridization and adaptive introgression in the evolution of irises (Iris; Arnold et al 2004), ecological divergence of sunflowers (Helianthus; Rieseberg et al 2007), and the signatures of divergent and balancing selection in campions (Silene; Minder and Widmer 2008) and poplar (Populus; Lexer et al 2010). So far, a few genes involved in adaptation or speciation have been identified in plants including hybrid sterility loci (Lexer and Widmer 2008), determinants of flower color-linked pollinator shifts (Hoballah et al 2007), and genes involved in hybrid necrosis (Bomblies and Weigel 2007).…”

What can patterns of differentiation across plant genomes tell us about adaptation and speciation?

“…These results suggest greater intraspecific variation for isolating factors than originally reported. Another study taking this genomic clines approach considered three hybrid zones between the European aspen species Populus alba and Populus tremula [43]. Circa onethird (33/93) of loci were high-divergence outliers, and two-locus epistasis was common.…”

Reproductive isolation of hybrid populations driven by genetic incompatibilities

“…If hybrid populations fixed for the parent species 1 genotype at one incompatibility pair and the parent species 2 genotype at the other, we considered the hybrid population as having evolved reproductive isolation from both parental species (albeit weaker than between the two parental species). While selection against hybrids will sometimes be so extreme that few hybrids will survive (or reproduce) in the population (see simulations below), selection against hybrids can also be more moderate, allowing hybrids to persist [41,45,[49][50][51][52][53]. In simulations of this moderate selection scenario, reproductive isolation between hybrid and parental populations can evolve frequently and rapidly (Fig.…”