Potential limits to the benefits of admixture during biological invasion

Abstract

Species introductions often bring together genetically divergent source populations, resulting in genetic admixture. This geographic reshuffling of diversity has the potential to generate favourable new genetic combinations, facilitating the establishment and invasive spread of introduced populations. Observational support for the superior performance of admixed introductions has been mixed, however, and the broad importance of admixture to invasion questioned. Under most underlying mechanisms, admixture's benefits should be expected to increase with greater divergence among and lower genetic diversity within source populations, though these effects have not been quantified in invaders. We experimentally crossed source populations differing in divergence in the invasive plant Centaurea solstitialis. Crosses resulted in many positive (heterotic) interactions, but fitness benefits declined and were ultimately negative at high source divergence, with patterns suggesting cytonuclear epistasis. We explored the literature to assess whether such negative epistatic interactions might be impeding admixture at high source population divergence. Admixed introductions reported for plants came from sources with a wide range of genetic variation, but were disproportionately absent where there was high genetic divergence among native populations. We conclude that while admixture is common in species introductions and often happens under conditions expected to be beneficial to invaders, these conditions may be constrained by predictable negative genetic interactions, potentially explaining conflicting evidence for admixture's benefits to invasion.

Keywords: cytonuclear interactions; epistasis; genetic diversity; heterosis; invasiveness; multiple introductions.

Fig 1.

Identifying the conditions under which admixture might be most favorable during invasions. Shown are predicted relationships for the performance of admixed populations as a function of (a) the genetic divergence between their source populations and (b) the genetic variation within their initial founding populations, under different genetic and evolutionary mechanisms. In a linear model of progeny performance in experimental crosses the invasive plant C. solstitialis (excluding heterotic outlier [Asia × southern Greece]), genetic divergence (interpopulation π) had a significant negative effect (c, P < 0.01) and genetic variation (intrapopulation π) in maternal populations had a significant positive effect (d, P < 0.001) on the deviation of progeny from mid-parent genotype expectations. Data points in (c,d) show progeny deviation from mid-parent as partial residuals after taking into account all other effects in the model. In the literature, genetic admixture in introduced plant populations is reported more often at intermediate genetic divergence (F_ST and related metrics for microsatellite markers) among potential source populations in the native range (e), and shows no relationship with average genetic variation (H_E) within native populations (f).

Fig 2.

Sampling sites and sequence variation in the native range of C. solstitialis. (a) Sampling sites for this study (large dots) span genetically divergent populations in western Europe (WE, blue), eastern Europe (EE, purple), southern Greece (SG, red), and Asia (AS, green) as previously identified from population genomic analyses (previous sampling indicated by large and small dots; Barker et al. 2017). (b) Average intrapopulation nucleotide diversity (π) across the total length of all ddRADseq reads within each sampling site (dots) and for all individuals pooled within a region (bars). (c) Average interpopulation π in pairwise comparisons between individuals from different populations.

Fig 3.

For each maternal region, panels (a−d) show growth rates of C. solstitialis progeny from experimental crosses to fathers from other regions and the mid-parent expectations for each cross. Growth rates are shown versus average pairwise nucleotide diversity (π) between parental populations. Color codes for each cross are as in Fig 2. Within-region crosses are indicated by solid colors, and between-region crosses by paternal region color outlined by maternal region color. Mid-parent expectations are shown as means (black bars) +/− s.e.m. (gray bars). Growth rates are least squares means +/− s.e.m., and significant deviations from mid-parent distributions are indicated as: *** P < 0.0001; ** P < 0.001; * P < 0.05.

Fig 4.

(a) Growth rates of C. solstitialis progeny from experimental crosses with all possible combinations of mother and father population-of-origin. Color codes for each cross indicate maternal and paternal population as in Fig 2, with paternal region color outlined by maternal region color. Growth rates are least squares means +/− s.e.m., and significant differences between reciprocal crosses of the same parental populations are indicated * P < 0.05. (b) In a linear model of progeny performance (excluding heterotic outlier [Asia × southern Greece]), growth rate of genotypes from the maternal region had a significant negative relationship (P < 0.0001) with the deviation of progeny from mid-parent expectations. Data in (b) show progeny deviation from mid-parent as partial residuals after taking into account all other effects in the model.