We have summarized evidence that, as a species becomes more common in a community, it will be more likely to interact with other conspecifics, as well as with specialized consumers and mutualists. On the other hand, as a species becomes rarer, it will increasingly interact with heterospecific competitors, and interact as well as with generalized consumers and mutualists, as their specialists leave or die out. We have also explored the potential evolutionary consequences of these changes, as these different ecological interactions are likely to select for different trait distributions (summarized in Fig. 2). Additionally, the density of a population will affect the efficiency with which that population can respond to selection, and this evolutionary response may in turn feedback to affect density. As conservation and natural resource management largely centers on manipulating the population size of target desirable or undesirable species, we must be aware of both the ecological changes that occur as a result and the evolutionary feedbacks generated by these changes.
Many of the ecological changes described earlier lead to negative feedbacks on species abundance that could act to prevent large fluctuations in species abundance. For instance, the density-dependent build up of specialized herbivores or pathogens may prevent a species from continually increasing in density, thereby maintaining diversity in the system (Janzen 1970). These shifting selective pressures may prevent directional evolutionary changes, as selection will never be consistent long enough to produce a sustained directional response (Bell 2010). However, in human-altered systems, these feedback processes may be interrupted, either with introduced species that lack diverse selective agents from the native range that impose checks and balances, or potentially also owing to much stronger and more directional selection imposed by human activities like harvesting or pesticides. (Hendry et al. 2008). The consequences of these actions may be that species experience persistently high or low densities, densities that might be uncharacteristic of that species’ evolutionary history and that may lead to consistent selection pressures and possibly evolutionary responses. We suggest that management practices may benefit from understanding the historical density of species and the evolutionary consequences of rapid and sustained density changes.
Newly rare: persistent low density
Much conservation research and practice is geared toward protecting species that exist at perennially low densities. Knowledge about the past commonness or rarity of a species may help predict the vulnerability of current populations to extinction. For some species, this rarity is the natural condition and thus these species likely have evolved traits appropriate to low conspecific density (Kunin and Shmida 1997). However, for other species, their current rarity is a novel condition driven by anthropogenic environmental changes, and managers should be aware that these species may have trait distributions that reflect their past environment, which included higher conspecific densities. Maladaptations of newly rare taxa may include defenses geared toward specialized rather than generalized enemies, or an overreliance on specialist mutualists that cannot maintain a viable population size at their host’s new, low density (Eckert et al. 2010). Additionally, animal species may have social traits that provide fitness benefits when group sizes are large (such as group vigilance or foraging) but that are ineffective or maladaptive below threshold conspecific densities (e.g., Roberts 1996). Such species may be at especially high extinction risks and would warrant special protection until their populations can rebound to historic levels or can evolve new trait values more appropriate for their new, low abundance (Honnay and Jacquemyn 2007). Again, managers must be aware that adaptation, including adaptation to rarity, may be slow and inefficient in small populations because of low genetic variation and strong genetic drift.
If low abundance threatens population persistence, then evolutionary rescue management options have sometimes been employed. Translocating individuals from other populations may be ineffective or even counterproductive, however, if those individuals are maladapted to the introduced environment. For instance, Weese et al. (2011) found that guppies from low-predation populations introduced to high-predation pools had minimal effects on population dynamics following a large disturbance because of strong selection against the migrants. While we know of no specific examples to date, it is possible that introducing individuals from a high-density population to a low-density one may introduce maladapted genes and lower average fitness. On the other hand, introducing individuals from populations with historically low density into populations that have suffered recent population declines may introduce alleles better adapted to the new low-density biotic interactions (as well as genotypes potentially less vulnerable to inbreeding depression).
Newly common: persistent high density
Natural resource managers are often faced with problematic species that maintain persistently high densities at the expense of more desirable species. Exotic invasive species are a clear example of this, as invasive populations behind the invasion front often achieve tremendously high densities. For many invaders, this high density appears stable, although the timescale of this stability (years, decades, centuries) is still unclear for many invaders (Simberloff and Gibbons 2004). Nevertheless, management may benefit from considering the unique selection pressures acting on such species that reach unusually high densities. By escaping their complex native communities, invaders may gain not just an immediate fitness benefit from reduced consumer loads, but also evolutionary benefits by escaping the conflicting selection pressure exerted by diverse consumers. If resistance to specialists trade offs with resistance to generalists, then invaders may be free to evolve very high levels of defense against generalists without incurring the costs of increased specialist loads (Joshi and Vrieling 2005). Thus, while native species must deal with fluctuating and conflicting selection from varying ratios of generalist and specialist enemies (Berenbaum and Zangerl 2006; Zangerl et al. 2008; Bell 2010), exotic invader populations may be free to adapt to more simplified selective regimes, may be able to reduce costs of these adaptations, and may increase in both fitness and abundance.
Changing encounter rates with conspecifics and heterospecifics, with concomitant altered selection, will occur as these invasive species increase in density. When a new invasive population is first established, either at the original introduction site or along the spreading invasion front, these newly dispersed individuals will be initially rare in their new community. As a rare member of the community, these new populations may be under selection for specific traits, including being highly competitive or aggressive against other species. It is these highly competitive/aggressive individuals that will be more likely to survive and reproduce and send propagules off to continue the expansion. This may lead to the evolution of ‘invasive’ phenotypes that excel at invading new communities and producing new colonists before their populations build up to a high level at any one invaded site. For instance, a study comparing populations of an invasive crayfish, Pacifastacus leniusculus, from its native and introduced ranges found invasive populations from streams with no native congeneric crayfish to be consistently more aggressive in their interactions with different crayfish species, as well as more voracious and active foragers and bolder in the face of predation risk (Pintor et al. 2008). As aggression, foraging rate, and boldness were correlated in these species, at high density, crayfish may be under selection to reduce their foraging rates and boldness to avoid costly aggressive interactions with conspecifics and congeners. On the other hand, invasive populations moving into crayfish-free streams may be released from this trade-off, because intraspecific interactions will be rare at least initially.
A similar process may occur in invasive plants that employ allelopathic traits to compete with heterospecifics. Allelopathy has been documented in a number of invasive plant species (Hierro and Callaway 2003) and may frequently create scenarios where the chemical traits are under different selection pressures based on the relative abundance of the allelopathic species (as described earlier for B. nigra). In a rapidly expanding allelopathic invader, one might predict selection for high allelochemical levels on the leading edge of the invasion, where competition is largely interspecific, but selection against the allelochemicals in well-established infestations if the invasive forms dense stands (resulting in high rates of intraspecific competition). Alliaria petiolata is an aggressive invader of forest understories in the eastern United States, and part of its invasive success may be because of its production of allelochemicals that negatively affect native plants and their mycorrhizal symbionts (Rodgers et al. 2008). If these allelochemicals are favored under inter-, but disfavored under intra-, specific competition, then one would expect to the see the genetic investment to the chemicals decline over time in populations as they build up density. Consistent with this prediction, Lankau et al. (2009) found a strong negative correlation between the allelochemical concentration of a population and its estimated age for 44 A. petiolata populations dated with herbarium records, indicating a trend for higher toxicity in newly established populations.
If the low initial relative abundance of invasive species tends to select for traits that make them better competitors with native species, then managers may need to consider how their management strategies affect these selection pressures. Most invasive species management is focused on reducing the abundance of the invader, following from the logical assumption that a smaller invader population should exert less impact on native species. However, by maintaining the invader population at a lower relative abundance, this management may also maintain the selection pressures on invader traits that are harmful to native species. As a preliminary exploration of this possibility, we surveyed the land owners/managers of the sites from which the 44 A. petiolata populations in Lankau et al. (2009) were collected. Of the 28 responders, 15 had performed no management of the A. petiolata population, and 13 had managed their invasion at some time in the past (mainly through hand pulling, with one case of herbicide spraying and one of weed whacking). For younger invasions, there was no difference in the allelochemical concentrations in managed or unmanaged populations (Fig. 3); in both cases, chemical levels were relatively high. For older invasions, chemical concentrations had dropped by about 40% in unmanaged populations. However, managed populations had maintained similarly high levels of the allelochemicals as the younger ones (Fig. 3). Thus, the pattern of declining allelochemical concentrations over time described in Lankau et al. (2009) appears to be only true for unmanaged populations. While many variables may be involved in this pattern, it is possible that by artificially maintaining the A. petiolata population at a lower relative abundance, management has maintained the selective value of high allelochemical concentrations. This could have consequences for native plants, as A. petiolata genotypes with higher allelochemical concentrations have stronger impacts on soil communities (Lankau 2010) and native plant growth (Lankau et al. 2009), and restoration of native tree seedlings is less successful in A. petiolata populations with high concentrations of glucosinolates (R.A. Lankau in review).
Figure 3. Mean and standard errors of root glucosinolate concentrations in Alliaria petiolata individuals from 28 populations grown in a common environment. Populations were divided into two age classes (estimated time since introduction to an area as determined by herbarium records) have either had no management (solid bars) or had been directly managed at some point in the past. Managed populations had significantly (P < 0.05) higher concentrations than unmanaged ones in the older, but not younger, age class. For more details, see Lankau et al. 2009.
Download figure to PowerPoint
Management strategies may invoke density-dependent selection even if they have little long-term effects on population densities. For instance, in California’s Central Valley, biocontrol agents released to control C. solstitialis (yellow starthistle) destroy 75% of seed produced, but C. solstitialis populations have not been strongly decreased by these agents to date (Garren and Strauss 2009). Self-thinning reduces seedling populations to the same adult densities, regardless of the presence of absence of the agent (Fig. 1). However, agents that dramatically reduce seed inputs may reduce intraspecific competition early in the life cycle and may favor traits in C. solstitialis that are more effective against interspecific native competitors (through reduced conspecific densities). To date, no one has examined the selective effects of biological control agents on traits of the target species as they relate to competitive ability with natives. Thus, by altering the intensity of intraspecific competition, agents may affect qualities of surviving plants, even if they do not affect final densities of these plants.
When will density-dependent selection matter for management?
Throughout this synthesis, we have advanced the argument that changes in the density and/or frequency of a population can have selective consequences mediated through interactions with conspecifics as well as other species. For managers and policy makers, it is important to know how frequently such selection can be expected and how strong these selection pressures will be relative to other forces acting on populations. Unfortunately, few data are available to address these questions directly. It is clear that when human activities impose direct selection on specific traits, such as body size in harvested fishes, evolutionary responses can be quite rapid (Darimont et al. 2009). It is likely the case that indirect selection imposed through changes in population density or frequency will be both weaker and less consistent, resulting in slower evolutionary responses (especially when density reductions result in loss of genetic variation and increased genetic drift). Nevertheless, many environmental changes and management practices have strong effects on density and no obvious direct selection on traits. We feel that in these scenarios, it is unwise to assume that there will be no evolutionary impact. We hope that future research will (i) determine traits under selection because of management-induced changes in density and community composition, (ii) quantify the strength of selection on these traits and compare this to direct selection imposed by management (i.e., harvesting, pesticides), and (iii) evaluate the ecological consequences of potential evolutionary responses for the focal species and its interacting community.