Recent admixture generates heterozygosity–fitness correlations during the range expansion of an invading species

Abstract

Admixture, the mixing of historically isolated gene pools, can have immediate consequences for the genetic architecture of fitness traits. Admixture may be especially important for newly colonized populations, such as during range expansion and species invasions, by generating heterozygosity that can boost fitness through heterosis. Despite widespread evidence for admixture during species invasions, few studies have examined the demographic history leading to admixture, how admixture affects the heterozygosity and fitness of invasive genotypes, and whether such fitness effects are maintained through time. We address these questions using the invasive plant Silene vulgaris, which shows evidence of admixture in both its native Europe and in North America where it has invaded. Using multilocus genotype data in conjunction with approximate Bayesian computation analysis of demographic history, we showed that admixture during the invasion of North America was independent from and much younger than admixture in the native range of Europe. We tested for fitness consequences of admixture in each range and detected a significant positive heterozygosity-fitness correlation (HFC) in North America; in contrast, no HFC was present in Europe. The lack of HFC in Europe may reflect the longer time since admixture in the native range, dissipating associations between heterozygosity at markers and fitness loci. Our results support a key short-term role for admixture during the early stages of invasion by generating HFCs that carry populations past the threat of extinction from inbreeding and demographic stochasticity.

Complex patterns of global spread in invasive insects: eco-evolutionary and management consequences

“…In the majority of cases where admixture is implicated, however, little evidence exists that the mixing of genotypes has had serious impacts on global invasiveness (Chapple et al 2013;Rius and Darling 2014). In addition, several of the studies that have detected positive effects of admixture attribute these to short-term heterotic effects rather than gains in additive genetic variation (Keller and Taylor 2010;Keller et al 2014), though this can still have important long-term consequences.…”

Reticulate evolution is favored in influenza niche switching

“…Beyond the viral world, recent reviews have asserted the importance of reticulate evolutionary events as a driver of speciation and niche diversification (22,23), and recent studies have illustrated heightened fitness effects in hybrid populations (24,25). However, none have quantitatively tested the importance of reticulate evolutionary strategies in enabling ecological niche switches on a global scale, especially in comparison with clonal adaptation under drift and selection (a task feasible only in fast-evolving organisms).…”

Investigating past range dynamics for a weed of cultivation, Silene vulgaris

“…Microsatellite amplification and fragment analysis were performed as described in Keller et al (2014). Genotyping and binning of the 167 new samples as well as an additional 79 samples from Keller et al (2014) was performed using GeneMarker 2.6.2 (Softgenetics, LLC, State College, PA). One marker, SL_eSSR17, was removed from the analysis due to peaks of varying sizes inconsistent with the known number of repeats.…”

“…We genotyped 10 of the 15 markers used in Keller et al (2014) and derived from S. latiolia as described by Moccia et al (2009; Table 1). Microsatellite amplification and fragment analysis were performed as described in Keller et al (2014). Genotyping and binning of the 167 new samples as well as an additional 79 samples from Keller et al (2014) was performed using GeneMarker 2.6.2 (Softgenetics, LLC, State College, PA).…”

“…Past genetic studies of S. vulgaris have found phylogeographic signatures of ancestral demes dispersed throughout Europe, making it difficult to predict past range dynamics (Taylor and Keller 2007;Keller and Taylor 2010;Keller et al 2014). Here, we add to the data from Keller et al (2014) by analyzing microsatellite data for additional samples with a greater representation of eastern and southern European populations from classic refugial areas (Iberia, Italy, Balkans).…”