Are there ecological consequences of vanishing proactive phenotypes?
Many studies have noted the essential role of keystone species that warrant specific conservation efforts due to their central position for the functioning of a community (Mills et al. 1993; Paine 1995; Betts et al. 2015), and whose extinction or massive population decline could have massive consequences on community structure (Cortés-Avizanda et al. 2015). Recent work has focused on the essential role played by some individuals in a group and coined the term keystone individuals (Modlmeier et al. 2014; Pruitt & Keiser 2014). Modelmeier et al. (2014: p55) defined these individuals as having “a disproportionally large, irreplaceable effect on other group members and/or the overall group dynamics relative to its abundance”.
The vanishing of proactive phenotypes could first have consequence in terms of group composition and population dynamics as these individuals are likely to be keystone individuals. As noted above, proactive individuals tend to disperse more, while reactive individuals are more likely to join newly colonized areas (Cote et al. 2010a). If new populations are composed only from reactive individuals, this may constrain dispersal and space use. For instance, group mean personality scores (boldness, activity, and sociability) of some feral guppy (Poecilia reticulata ) populations was not associated with exploratory propensity. Rather, group exploratory propensity was driven by the personality of key individuals whereby slow individuals tended to slow down exploration rates of the shoal (Brown & Irving 2014). In mosquitofish (Gambusia affinis ) mean group personality appeared to also drove group dispersion patterns in the expected pattern (group with many asocial individuals disperse further) although there were no keystone individuals identified (Cote et al. 2010b). Because exploration is likely associated with resource harvesting patterns, we can envision that HIREC may modify these patterns and have consequences at other trophic levels. Thus, if a system evolved with a mix of shy and bold individuals, and HIREC systematically eliminated one type, we should expect changes in species composition.
The disappearance of one phenotype could also have substantial consequences on prey-predator relationships. In a recent review, it was considered that a proactive or a reactive response of a prey largely depends on the predictability of an encounter with a predator (Creel 2018). The former response will have an energetic cost (fleeing) while the latter would have stress-mediated cost, by activating the HPI/A axis (Creel 2018). However, this approach largely ignored intrinsic differences in coping abilities between individuals of the same species and rather considered that all individuals are able to mount a similar response according to the situation. Here we suggest that the type of response would also depend on the personality of each individual, although ecological consequences would be the same. If proactive individuals vanish from the population, then responses to a predator consisting of displaying aggressive behavior, modifying activity periods, or engaging in particular patterns of vigilance (Creel 2018) would likely be quite different. Rather, the reactive response will be systematically produced, with all its associated stress-related costs. For instance, in the snowshoe hare-lynx system, predation risk increased glucocorticoid production with direct consequences in the decline of offspring production (Krebs et al. 1995). Hence, we can expect that always mounting a reactive response to predatory encounters would lead to chronic stress and its associated consequences in terms of reproductive success.
We know that behavioral variation is an index of genetic variation (Smith & Blumstein 2013). If we selectively reduce phenotypic variation, we are likely reducing genotypic variation. Such a reduction may be ultimately costly if it reduces a population’s adaptive potential to what may ultimately be a more variable environment. This loss of behavioral diversity may be particularly acute in conservation management when animals are brought into captivity for breeding with subsequently planned translocations and reintroductions (e.g., Smith & Blumstein 2012; Merrick & Koprowski 2017). We expect captivity to reduce genetic variation and also to eliminate the very variation that may be essential for the wild.