Dispersal in the course of an invasion


Arne W. Nolte, Fax: ++49 4522 736 281; E-mail: nolte@evolbio.mpg.de


Invasive species receive attention as manifestations of global ecological change and because of the effects that they may have on other organisms. They are commonly discussed in the context of the ecological perturbations or the human activities that permitted the invasion. There is also evidence, that there is an intrinsic component to biological invasions in that evolutionary changes of the invaders themselves can facilitate or limit invasions (Lee 2002; Urban et al. 2007; Van Bocxlaer et al. 2010). Hence, teasing apart whether environmental change or changes of the organism foster invasions is an interesting field of research. Ample evidence for plants and animals documents that ecological change and human activities trigger range expansions and invasions, but questions regarding evolutionary change of invaders remain less explored although there are several reasons to believe it matters. Firstly, rapid evolutionary change is possible in timeframes relevant for contemporary biological invasions (Hendry et al. 2007). Furthermore, population genetic modelling suggests that there are circumstances where the range expansion and colonization of empty spaces in the course of an invasion can induce evolutionary change in a way that is specific to invaders: the process of repeated founding out of marginal populations in the course of a range expansion can shift allele frequencies and has been referred to as allele surfing, which not only affects neutral genetic variance, but also fitness relevant traits (Klopfstein et al. 2006; Travis et al. 2007; Burton & Travis 2008). Importantly, this process poses a null model for evolutionary inference in invasive populations. It predicts conspicuous allele frequency changes in an expanding metapopulation unless migration homogenizes the gene pool. Despite this relevance, ideas about allele surfing rely heavily on modelling although some experimental evidence comes from studies that document the segregation of genetic variants in growing plaques of bacteria (Hallatschek et al. 2007). To date, little empirical data is available that would reveal the migration processes that affect the establishment of gene pools at invasion fronts in natural systems. This aspect sets the study of Bronnenhuber et al. (2011) apart. They quantify migration behind the expansion front of an invading fish and thus provide important baseline data for the interpretation of the emerging patterns of genetic differentiation.

The authors study dispersal in an expanding metapopulation of the Ponto – Caspian round goby Neogobius melanostomus, an invader in the Great Lakes region in North America (Fig. 1). The invasion is very recent and well documented so that the dispersal dynamics at the expansion front can be observed as the range expansion occurs. They have sampled multiple sites over a period of several years in three tributaries to the Great Lakes and typed 1262 individuals for eight microsatellite markers. The authors find a consistent genetic structure that is mostly stable in consecutive years and differentiation occurs particularly among distant or isolated localities which supports that the dataset as such is informative. Given a detectable genetic structure, genotype assignment can be used to infer the origin of individuals and hence, to infer patterns of migration. The authors study the relative role of long range vs. short range dispersal. Some migrants can be identified and these suggest that long range dispersal can play a role to shape the gene pool. Further, this finding is in line with the idea that different individuals may follow alternative dispersal strategies and it is possible that round gobies vary greatly in their migratory behaviour and site fidelity. On other hand complex processes determine the fate of larvae of riverine fishes. Particularly when juveniles go through a pelagic phase as is the case in round gobies they can be expected to be washed downstream with the current. Juveniles apparently migrate towards surface waters at night which contributes to the spread of gobies within the Great Lakes system (Hensler & Jude 2007). Conversely, downstream drift has to be compensated by upriver migration to explain an upriver population expansion. Hence, it is obvious that dispersal may be influenced by chance and complex behaviors and Bronnenhuber et al. (2011) provide an insight into the dispersal distances and directions that can be realized by round gobies.

Figure 1.

Round gobies (Neogobius melanostomus) originate from Black Sea drainages and have recently invaded vast areas in Europe and in North America. While the invasion as such is a threat to local ecosystems, invasive species also represent success stories in a time of global ecological change. They may illustrate what makes a species successful while others disappear (Photo: Stan Yavno).

There are uncertainties with the analysis that can be expected to represent a general dilemma in analyses of invasive species: While the statistical analysis of the authors is very useful, recent origin and divergence among populations of round gobies results in low levels of genetic differentiation in several population comparisons, which reduces the power to correctly assign individuals (Bernatchez & Duchesne 2000). Moreover, the relative effect that stochastic errors in the sampling of multilocus genotypes or genotyping errors will have on the correct assignment is more severe the less pronounced the overall genetic differentiation is. Yet, there is a flip side to a possibly reduced assignment success: if some immigrants can be identified, then one can assume that the true migration rate may be higher to the extent that there is a lack of power to detect migrants. It may thus turn out that the amount of migration that can be detected underestimates the true migration rate by far, especially among genetically similar populations.

Besides representing a severe problem in conservation biology, invasive populations where high gene flow prevails could turn into interesting systems to study the evolutionary trajectories of invasive species (Lee 2002; Haenfling 2007; Gomulkiewicz et al. 2010). This is because population genetic signatures of adaptive evolution can be expected to emerge while neutral changes in local allele frequencies are suppressed by high dispersal. Such a situation could be given in round gobies (Bronnenhuber et al. 2011) or in the cane toad in Australia (Leblois et al. 2000). To this end, the authors describe an intriguing amount of heterogeneity in the metapopulation despite the extremely recent origin of the populations the Great Lakes region. This could be explained by independent introductions of different strains or isolated founding events at multiple sites. Indeed, the available evidence suggests that the round goby invasion was seeded by a genetically diverse stock (Dillon & Stepien 2001). The patterns of migration now observed by Bronnenhuber et al. (2011) may ultimately result in an erosion of the currently observed structure. On other hand, it may turn out that gene flow through genetically divergent immigrants may be constrained through emerging local adaptation as suggested for migrants in Atlantic salmon (Dionne et al. 2008). It will be exciting to follow up in the future whether or not we observe a trend to increase or decrease population structure in invasive gobies which will give us hints about adaptive evolution in the course of the invasion.

A.N. is interested in how fishes evolve as a consequence of interactions with their environment. He studies natural hybridization in nature and in the lab in order to identify the genetic basis for differences between species.