Box 1 Bottlenecks and Mendelian trait variation
Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions
Article first published online: 1 OCT 2007
© 2007 The Authors. Journal compilation © 2007 Blackwell Publishing Ltd
Volume 17, Issue 1, pages 431–449, January 2008
How to Cite
DLUGOSCH, K. M. and PARKER, I. M. (2008), Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Molecular Ecology, 17: 431–449. doi: 10.1111/j.1365-294X.2007.03538.x
Molecular markers are discrete traits with Mendelian inheritance, and therefore traditional population genetic theory easily generates predictions about their response to demographic bottlenecks. Nei et al. (1975) showed that the loss of genetic diversity is governed by the effective minimum (or founder) population size (Ne) and the growth rate of the population. Lower Ne and/or growth rate will lead to the loss of more alleles, particularly those that are rare. Experimental and observational work has since supported these predictions (e.g. McCommas & Bryant 1990; Leberg 1992; England et al. 2003; Eldridge et al. 2004). Rare alleles that persist through a bottleneck have the opportunity to become more common, and in general, large shifts in allele frequencies are predicted. For molecular markers, we expect most of these shifts to have no effect on fitness. For other types of Mendelian traits, however, the evolutionary importance of shifts in allele frequencies and losses of rare alleles is likely to be highly idiosyncratic. While many rare alleles are deleterious, a few, particularly those under frequency dependent selection, may have important fitness consequences (e.g. sex-determining alleles in fire ants, Ross et al. 1993; self-incompatibility alleles in plants, Elam et al. 2007).
Multiple introductions are predicted to augment Mendelian trait diversity in founding populations by raising both Ne and population growth rate, but even greater increases can be realized if there is differentiation across the geographical distribution of populations in the source region (Ellstrand & Schierenbeck 2000). This is especially true for inbreeding or exclusively clonal species (particularly plants), where native genetic diversity is expected to be low within populations but high among them (Gray 1986; Hamrick & Godt 1989; Barrett & Husband 1990; Schoen & Brown 1991). In these cases, within population diversity is not likely to be unusually low in bottlenecked invasions (just similarly low), and it can easily be higher, if an intentionally mixed stock or multiple introductions combine genotypes from differentiated source populations (Novak & Mack 1993; Novak & Mack 2005).
Box 2 Bottlenecks and quantitative trait variation
Quantitative traits integrate across the effects of multiple genes and are characterized by distributions rather than discrete trait values. The portion of a distribution that can be attributed to additive variance is critical for determining the response to selection, since only additive gene action translates parental traits directly into offspring traits. Reductions in additive variation due to demographic bottlenecks are expected to be small, because distributions of quantitative variation are relatively insensitive to the loss of rare alleles (Lande 1980; Barton & Charlesworth 1984). Furthermore, additive variation may increase after a bottleneck due to frequency shifts at loci with nonadditive gene interactions, converting epistatic or dominance variance to additive variance (Goodnight 1988; Whitlock et al. 1993; Willis & Orr 1993; Cheverud & Routman 1996; Wang et al. 1998; Kirkpatrick & Jarne 2000; López-Fanjul et al. 2002; Naciri-Graven & Goudet 2003; Zhang et al. 2004; Turelli & Barton 2006; Van Buskirk & Willi 2006; Willi et al. 2006). Such increases in additive variation have been observed under experimental conditions, particularly for life-history traits, which are expected to have many nonadditive genetic components (reviewed in Neiman & Linksvayer 2006). Examples from natural systems are rare; however, in a recent study, higher additive variation was coupled with evidence of a bottleneck in island populations of Rana arvalis (Knopp et al. 2007).
These gene interactions, as well as the action of selection, can decouple patterns of quantitative variation from those of discrete molecular markers. This decoupling can make molecular markers poor predictors (typically underestimates) of evolutionary potential in important fitness-related traits (Barrett & Richardson 1986; Pfrender et al. 2000; Merilä & Crnokrak 2001; Reed & Frankham 2001; McKay & Latta 2002), though few studies have adequately addressed this comparison (Crnokrak & Merilä 2002; Latta & McKay 2002). Nevertheless, neutral molecular markers should reflect total losses of genetic variation, which may ultimately affect the potential for quantitative traits to achieve extreme phenotypes. For example, Briggs & Goldman (2006) found that bottlenecked populations of Brassica rapa initially responded more quickly to artificial selection than did stable populations, but were ultimately more limited in their long-term response. The trade-off between loss of total variation and gain of additive variation has not been explored in natural populations and deserves further attention (Lee 2002). Perhaps the additional genetic diversity contributed by multiple introductions over the long-term will be crucial for sustained adaptive change in founding populations.
Box 3 The challenge of making relevant comparisons with source regions
There are many key questions in invasion biology that rely on comparisons between the native range and the introduced range (Hierro et al. 2005). These comparisons are often made by sampling broadly across the native range; however, the entire native range is not the most appropriate comparison for certain types of questions. In particular, to study the genetic changes that may have occurred during and after the introduction process, it is important to identify with as much precision as possible what was the original source for the introduction. Because the source region provides the benchmark against which genetic and evolutionary changes are assessed, it must represent variation from which an introduction was actually derived, otherwise apparent evolutionary changes since introduction may simply reflect regional differences (i.e. local adaptation, drift, and evolutionary history) between the true source population and the area sampled for study. For this same reason, comparisons between introductions and populations from across a broad source region may obscure important changes in the introductions that appear small against the range of variation in the source region.
Unfortunately, reliable records of the precise origins of introduced populations do not exist for most invaders. Instead, we typically rely on surveys of molecular variation to identify regions that are likely to contain the source of a particular introduction. The accuracy of this approach will be determined by the intensity of sampling in introduced and source areas, by the resolution of the molecular markers involved, and by the scale of differentiation across the potential source area. Future studies that pay close attention to these issues will offer particularly meaningful insights into the evolutionary ecology of introduced species.
- Issue published online: 1 OCT 2007
- Article first published online: 1 OCT 2007
- Received 19 March 2007; revision received 3 July 2007; accepted 8 August 2007
- exotic species;
- genetic bottlenecks;
- local adaptation;
- molecular diversity;
- non-native species;
- quantitative trait evolution
Invasive species are predicted to suffer from reductions in genetic diversity during founding events, reducing adaptive potential. Integrating evidence from two literature reviews and two case studies, we address the following questions: How much genetic diversity is lost in invasions? Do multiple introductions ameliorate this loss? Is there evidence for loss of diversity in quantitative traits? Do invaders that have experienced strong bottlenecks show adaptive evolution? How do multiple introductions influence adaptation on a landscape scale? We reviewed studies of 80 species of animals, plants, and fungi that quantified nuclear molecular diversity within introduced and source populations. Overall, there were significant losses of both allelic richness and heterozygosity in introduced populations, and large gains in diversity were rare. Evidence for multiple introductions was associated with increased diversity, and allelic variation appeared to increase over long timescales (~100 years), suggesting a role for gene flow in augmenting diversity over the long-term. We then reviewed the literature on quantitative trait diversity and found that broad-sense variation rarely declines in introductions, but direct comparisons of additive variance were lacking. Our studies of Hypericum canariense invasions illustrate how populations with diminished diversity may still evolve rapidly. Given the prevalence of genetic bottlenecks in successful invading populations and the potential for adaptive evolution in quantitative traits, we suggest that the disadvantages associated with founding events may have been overstated. However, our work on the successful invader Verbascum thapsus illustrates how multiple introductions may take time to commingle, instead persisting as a ‘mosaic of maladaptation’ where traits are not distributed in a pattern consistent with adaptation. We conclude that management limiting gene flow among introduced populations may reduce adaptive potential but is unlikely to prevent expansion or the evolution of novel invasive behaviour.