To the edge: studies of species’ range limits

A fundamental goal of ecology and evolution is to explain patterns of species' distribution and abundance (Elton, 1930). The range boundary presents a rather clear-cut setting in which to study determinants of distribution and abundance because a species is present on one side of the (usually fuzzy) boundary and absent on the other. A second reason for the interest in distribution limits is more practical and concerns species' accommodation to rapid climate change and disturbance – will species move to track their environmental niche or will they adapt in response to changing conditions? Even environmental tracking ultimately requires some level of evolutionary adaptation because not all conditions will be the same in the 'new' range (Griffith & Watson, 2006; Visser, 2008). The article by Darling et al. (this issue, pp. 424–435) examines potential limits to range expansion as a result of colonization-related traits in populations at the range edge. 'Darling et al. have flipped the question of dispersal limitation on its head ...' From an ecological and evolutionary perspective, there are four hypothesized causes for limits on range expansion. The first two causes are genetic and reflect sources of constraint on adaptive evolution at the range edge, and all but the last cause are predicated on the assumption that environments deteriorate towards and beyond the range boundary. According to the first hypothesis, a species fails to adapt to adverse abiotic or biotic environmental conditions because of low levels of genetic variation or covariation in ecologically important traits in range-edge populations (Hoffman & Blows, 1994; Blows & Hofmann, 2005). Limited genetic variation results from genetic drift and low mutational input in small populations (discussed later under demographic limits) or because of strong selection at the range edge (Kirkpatrick & Barton, 1997). The second hypothesized constraint comes from contamination of range-edge gene pools by maladapted 'center' alleles because of biased gene flow from the center to the edge of the range (Kirkpatrick & Barton, 1997; Gomulkiewicz et al., 1999). Under some circumstances, however, center-to-edge gene flow can rescue edge populations from limited genetic variation and permit adaptive evolution (Holt & Gomulkiewicz, 1997). The third possible cause of limitation is demographic. Demographic limits are also based on deteriorating conditions at the range edge that, in turn, lead to low population growth, small population size and a high extinction rate. Populations persist at the range edge because of colonization from central populations but never build up to a size sufficient for further expansion (Pulliam, 1996). Edge populations are 'sinks' that owe their persistence to central 'source' populations. Genetic and demographic limits clearly are not independent of one another, as population size affects genetic variation and fitness affects population growth rate and size, as well as the carrying capacity of the environment (Holt & Gomulkiewicz, 1997). Finally, limits to range expansion can simply reflect geographic history, if a species has not yet arrived beyond its present boundary because of short-term or long-term colonization barriers. In such cases, the range edge is not in equilibrium. The spread of invasive species clearly illustrates the importance of dispersal barriers as a cause of prior range limits. Darling et al. have flipped the question of dispersal limitation on its head to ask whether range-edge populations of Abronia umbellata (Nyctaginaceae) have diverged, through adaptive evolution, from central populations to increase their colonizing ability. A. umbellata is limited to a very narrow band of coastal dunes but has a very large north–south distribution along the Pacific coast of North America (Fig. 1a). Darling et al. compared northern, southern and central populations for seed-dispersal ability and for floral traits affecting the ability of plants to self-pollinate. Self-pollination allows plants to colonize and reproduce in new locations in the absence of conspecific mates (Baker, 1955). Darling et al. found that the ability of seeds to disperse (Fig. 1b) and of flowers to self-pollinate (Fig. 1c) is higher in range-edge populations than in central populations. Photograph of Abronia umbellata plants at Camp Pendleton Marine Corps Base (San Diego County, CA, USA) (a); variation in seed morphology (wing area to seed mass) related to dispersal ability (b); and variation in flower size (c). Images courtesy of C. Eckert (Queen's University, Kingston, Canada). Theoretical predictions on the advantage of dispersal are complex and depend on whether environments deteriorate at the range edge, on the direct effects of selection for greater or lesser dispersal at a local spatial scale, and on indirect effects of local selection at broader spatial scales (Holt, 2003). If the range edge is dynamic (i.e. not at equilibrium) or environmental quality does not vary, greater dispersal ability is likely to be favored. With environmental degradation, dispersal is probably disadvantageous, unless there is strong local competition or spatial/temporal environmental variation at the source. Evidence of greater dispersal ability at range margins is accumulating and has been reported previously in plants (e.g. Cwynar & MacDonald, 1987) and animals (e.g. Hill et al., 1999), in native and nonnative species, and in species with expanding and stationary ranges. Whether this pattern simply reflects the fact that individuals which are good dispersers, both genetically and phenotypically, arrive at range edges sooner and more frequently than poor dispersers, or whether there has been in situ selection for increased dispersal, is not always clear. Rapid genetic divergence has been observed in morphology, phenology, physiology and behavior in both native and nonnative species with expanding ranges (e.g. Maron et al., 2004). There is no reason to think that the evolution of dispersal ability should be an exception. The evolution of traits that increase self-fertilization (e.g. the loss of self-incompatibility and reduced protandry and herkogamy) has been reported frequently in plant taxa that occupy geographical or ecologically marginal locations (see Runions & Geber, 2000 for review). Similar geographic patterns, involving the evolution of asexual reproduction, have been reported in plants (Bierzychudek, 1985), invertebrates and vertebrates (e.g. Kearney et al., 2006). Consistent with Baker's (1955) hypothesis that selfing and asexual reproduction enhance colonizing ability, Darling et al. report a decline in herkogamy, self-incompatibility and flower size in range-edge compared with central populations of A. umbellata. It should be pointed out that floral traits indicative of self-pollination do not always correlate with increased selfing. For example, Herlihy & Eckert (2005) found that geographically marginal populations of Aquilegia canadensis had reduced herkogamy and smaller flowers, but very similar outcrossing rates, relative to central populations. Empirical studies that test the rich body of theory on the ecology and evolution of range limits are slowly accumulating, but much remains to be established. For example, the simple assumption that abiotic or biotic environments deteriorate from range center to edge has rarely been tested. It is not sufficient to document environmental gradients or to circumscribe the geographic range of a species within a set of environmental parameters (i.e. delimit the environmental niche); the species' response to environments at the center, margin and beyond the range edge must be assessed, and this requires transplant experiments. Where transplants have been carried out (see Gaston, 2003; Angert & Schemske, 2005; Geber & Eckhart, 2005; Griffith & Watson, 2006; Samis & Eckert, 2007), fitness has been found to decline beyond the range boundary in only half of the cases. It is surprising that in the face of hundreds of reciprocal transplant studies assessing local adaptation and ecotypic differentiation within a geographic range (Linhart & Grant, 1996), so few studies have included the range boundary. Theoretical models on distribution limits are as applicable to habitat boundaries as to range boundaries, yet we know comparatively little about the spatial scale of adaptation – are fitness declines across range boundaries, where they occur, comparable with those across habitat boundaries? Demographic data on central populations and range edge populations are relatively scarce, and here again, only a subset of studies report that populations are smaller and more sparsely distributed at the edge compared with the center of the range, as predicted by the scenario of environmental deterioration (Sagarin & Gaines, 2002; Samis & Eckert, 2007). Few data exist on the temporal and spatial dynamics of populations across a geographic range (but see e.g. Angert, 2006). Are range edge populations sinks? Do they exhibit metatpopulation dynamics? We are equally ignorant of genetic constraints in range expansion. While there are many reports of lower levels of molecular variation and greater population differentiation in peripheral compared with 'core' populations, there are many fewer studies of levels of quantitative genetic variance or co-variation in traits related to adaptation at range margins (Blows & Hofmann, 2005). Lastly, it remains a wide open question of whether gene flow from central to peripheral portions of a species' range is of sufficient magnitude to limit or spur adaptive evolution at range margins (Bridle & Vines, 2006).

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