Begging for a better future: how far can behavioral ecologists go without specifying mechanisms?

Abstract

Mock et al.’s critical review of the ‘‘honest begging’’ literature is certainly welcome and constructive. We agree that there are some problems with Signal of Need (SoN) including its interactions with Signal of Quality (SoQ) (Lotem 1998), and the fact that it makes opposing predictions for different fitness functions (Cotton et al. 1999) and ‘‘assumes away’’ the dynamic nature of parent–offspring interactions (Godfray and Johnstone 2000). We are obviously pleased with the endorsement of the fuel gauge model (FGM; Grodzinski and Lotem, 2007) but feel that its presentation as a version of the Signaling of Hunger idea (SoH), that is, as an alternative to SoN, gives it a different interpretation than originally intended. The distinction may look subtle but it is critical: In our view, the field does not require another normative model but crucially requires mechanistic models connecting the theoretical terms ‘‘need’’ and ‘‘quality’’ with biological reality. The FGM is therefore not an alternative to SoN, but a mechanistic model explaining how food deprivation can cause a gradual increase in need (i.e., in the marginal fitness value of receiving extra resources). The first component of the FGM is that sated (full) offspring have a need level of zero simply because they are not receptive to being fed, so food cannot be converted into offspring fitness. However, this food-receptivity component, termed ‘‘being ready for additional food’’ by Mock et al., is not sufficient to explain further increases in begging with food deprivation (receptivity alone could be indicated by an allor-none signal or cue). This is where the second component of the FGM becomes essential. The reason that an ‘‘almost empty’’ offspring is needier than a ‘‘half empty’’ offspring is that although they may be equally ready to receive a meal, the almost empty one is at greater risk of becoming completely empty, which might temporarily stop its ‘‘digestive engine’’ converting food into growth (Grodzinski and Lotem 2007). Alternatively, ‘‘efficiency-based’’ models suggest that fullness reduces digestive efficiency, providing a different functional reason for why food-deprived offspring will gain more fitness from being fed (Grodzinski and Lotem 2007; Wright et al. 2010). Importantly, specifying the alternative mechanisms through which SoN may work enables us to return to ultimate reasoning with relevant experimental results (Grodzinski et al. 2009). If the justified criticism of being ‘‘content with SoN’’ leads to this integrating approach, as we suggest, we are not really ‘‘expanding from signal of need,’’ but breaking it down to concrete examples that can be studied and understood at the mechanistic level. In contrast, using ‘‘hunger’’ or ‘‘fullness’’ without clarifying their relation to fitness might not take us much further than need or quality. We greatly sympathize with Mock et al.’s call to move beyond the ‘‘hunger experiment’’ and the honest signaling preoccupation but feel that expanding to SoH or SoQ may not be the best way. In theory, begging should be adjusted in relation to both differential costs (quality) and benefits (need), but offspring must assess those through proximate factors, such as digestive physiology, hormonal levels, competitive state, and past experience. Understanding these mechanisms is necessary for decoding the message conveyed by begging and assessing the extent to which begging is honest and parental response to it is adaptive. On the bright side, it seems that the field is already moving in this direction with an increasing number of studies into the genetic and phenotypic mechanisms of parent–offspring communication (e.g., Bell 2008; Grodzinski et al. 2008; Dor and Lotem 2009, 2010; Hinde et al. 2009; Wright et al. 2010). We should perhaps recall that the honest-signaling revolution was mainly a conceptual one. It provided a stable solution for the problem of cheating, facilitating the use of normative models like those used for animal foraging to study animal communication. Now that behavioral ecologists gradually stopped asking whether foraging is optimal and are instead using optimality as a working hypothesis for studying the evolution of behavioral mechanisms (recently reviewed by McNamara and Houston 2009), we can stop asking whether begging is honest as a goal in itself. Instead, we can use working hypotheses about costly signaling and evolutionary stability (implying some general concept of honesty) to study the mechanisms that make offspring begging and parental response to it adaptive.