Adaptive Genetic Differentiation of Invasive Species; Slender False Brome as a Model

Abstract

It has been difficult to identify unifying characteristics that would allow prediction of invasiveness, but the most aggressively invasive species often have relatively high genetic diversity in their introduced range, suggesting they were established by multiple introductions. The invasive slender false brome (Brachypodium sylvaticum) provides a well‐studied example to understand how multiple introductions leads to invasiveness. Genetic admixture among divergent varieties of this species from the native range provided high levels of diversity and facilitated adaptive evolution for increased drought tolerance. Range expansion produced less vigorous inbred populations, but gene flow appears to alleviate inbreeding depression through the introduction of genetic variation followed by selection for purging of genetic load. Human‐mediated dispersal has facilitated the spread of false brome by concentrating seed deposition in areas that have been disturbed. The success of invasive species may provide us with models for the management of native species declining due to climate change.

Key Concepts

  • It has been difficult to identify any unifying characteristics of introduced species that would help predict their potential to become invasive.
  • One commonality for many of the most aggressively invasive species is high genetic diversity in their invaded range, which suggests that they were first established by multiple introductions.
  • The Brachypodium sylvaticum (slender false brome) invasion provides a well‐studied example of how multiple introductions can promote adaptation and invasiveness.
  • Cultivation of divergent lineages of B. sylvaticum by range managers in the same location promoted admixture and the generation of hybrid invasive lineages.
  • Comparison of phenotypic and genetic marker variation between the introduced and native ranges provides evidence of adaptive divergence for traits associated with drought tolerance.
  • The spread of B. sylvaticum was facilitated by its association with human activity producing long‐distance seed movement and directed dispersal resulting in high propagule pressure.
  • Inbreeding depression in newly colonised populations at the expanding range edge may be overcome by purging of genetic load due to gene flow among populations followed by selection.
  • The rapid adaptation facilitated by admixture in invasive species may provide a model for management strategies for native species under pressure from climate change.

Keywords: adaptation; admixture; gametic (linkage) disequilibria; directed dispersal; genetic load; hybridisation; inbreeding depression; invasive species; isolation by resistance (IBR); purging

Figure 1. Examples of forest understory before and after invasion by Brachypodium sylvaticum (slender false brome). Prior to invasion the understory is typically a rich mixture of shrubs, ferns and herbaceous perennials (left; photo by Miguel V.). Photo on the right shows a heavily invaded region of the McDonald‐Dunn Experimental Forest near Corvallis, Oregon (photo by Alisa Ramakrishnan). The inset photo is by Glenn Miller. Cruzan . Reproduced with permission from Oxford University Press.
Figure 2. History of the introduction and range expansion of Brachypodium sylvaticum based on herbarium collections (red triangles). Data were compiled by Alisa Ramakrishnan. Cruzan . Reproduced with permission from Oxford University Press.
Figure 3. The probabilities of genetic contribution of native populations to the Brachypodium sylvaticum (slender false brome) invasion in Oregon. Marchini et al. . Reproduced with permission from John Wiley & Sons.
Figure 4. Comparison of statistical tests for differences between means (ANOVA) to the test for trait differences relative to the level of genetic differentiation (QST – FST). Selection may make trait means either more similar (QST < FST; upper comparisons – homogenising selection) or less similar (QST > FST; lower comparisons – diversifying selection) than expected based on the expected value based on no selection (i.e. QST = FST). Marchini et al. , Figure S4. Reproduced with permission from John Wiley & Sons.
Figure 5. When a subset of populations contribute to the establishment of a new population we expect both the mean of quantitative traits and the allelic composition of neutral genetic markers to be similarly influenced by the relative contributions (weights) of the source populations. In this scenario, the mean of all possible source populations (X) is substantially different than the weighted mean (Xw) upon initial colonisation. We can make a more robust test to detect evolution in the invaded range by comparing observed trait values to the expected mean based on source contributions. Marchini et al. , Figure S1. Reproduced with permission from John Wiley & Sons.
Figure 6. Responses of functional traits to selection for drought adaptation in the invaded range in the Pacific Northwest of North America for Brachypodium sylvaticum. Each graph compares the means of an individual trait between plants of invasive (orange) or native (green) origin. Asterisks indicate significant differences between means, and vertical lines represent the standard error of each mean. The arrows to the right of each graph indicate the expected change in response to increased drought tolerance. Cruzan . Reproduced with permission from Oxford University Press.
Figure 7. A simulation of range expansion after introduction of several genetically divergent lineages. The initial range expansion is slow as genetically differentiated lineages spread (a). Purging of genetic load begins where divergent phalanxes come into contact (b and c). Range expansion accelerates as the newly purged lineages spread (d). Each cell is a separate population. Warmer colours indicate lower population genetic load. Marchini et al. . Reproduced with permission from Springer Nature.
Figure 8. Multiplicative fitness for offspring from self (blue) and outcross (green) pollinations to plants of Brachypodium sylvaticum from its invaded range in Oregon, USA. The heterozygosity (He) of each population is represented by red markers with vertical lines indicating the error among microsatellite loci. Multiplicative fitness is estimated as the product of seed germination, early growth, survival and biomass. Vertical bars for fitness means represent the standard errors. Marchini et al. . Reproduced with permission from Springer Nature.
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Further Reading

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Cruzan, Mitchell B(Sep 2019) Adaptive Genetic Differentiation of Invasive Species; Slender False Brome as a Model. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0028733]