In their broadly relevant target article, Anselme & Güntürkün (A&G) point out that animals, particularly small passerines, are remarkably responsive to unpredictable food sources, eating and storing more food when access to it is limited or unreliable. The authors convincingly link this behavior to an adaptive evolutionary strategy to prevent death by starvation, which would certainly impose a large fitness cost on animals of reproductive age or younger. Here, we aim to extend the argument of A&G by highlighting another potential fitness cost to food unreliability for small passerines, even if the birds survive. Oscine songbirds, a clade that makes up approximately 80% of passerine species, learn their song from an adult tutor, and females use the quality of a male's song to assess his potential as a mate (Byers & Kroodsma Reference Byers and Kroodsma2009; Catchpole & Slater Reference Catchpole and Slater2003; Nowicki et al. Reference Nowicki, Searcy and Peters2002b). Importantly, reduced access to food early in development is linked to a reduction in song quality: When juvenile birds experience elevated stress levels because of food restriction or high parasite load, they produce lower-quality songs in adulthood, presumably because the stress has impeded development of the neural pathways underlying song learning (MacDonald et al. Reference MacDonald, Kempster, Zanette and MacDougall-Shackleton2006; Schmidt et al. Reference Schmidt, MacDougall-Shackleton, Kubli and MacDougall-Shackleton2014; Spencer et al. Reference Spencer, Buchanan, Leitner, Goldsmith and Catchpole2005).

In addition, stress during development has been linked to reduced fitness, measured by increased mortality and decreased reproductive output (Blas et al. Reference Blas, Bortolotti, Tella, Baos and Marchant2007; Gorman & Nager Reference Gorman and Nager2004). Taken together, these studies suggest that song-learning prowess in birds is linked to their access to food early in life, which, by extension, implies that learned vocalizations can be honest signals of fitness due to the effects of nutritional stress (Buchanan et al. Reference Buchanan, Spencer, Goldsmith and Catchpole2003; Nowicki et al. Reference Nowicki, Searcy and Peters2002a) In this sense, food instability is particularly impactful when passerine birds are raising offspring. If birds raise their chicks in times of limited food availability, the resulting stress can make their offspring less sexually attractive even if food is subsequently becomes abundant and predictable. An increase in foraging behavior in such an environment may protect against this potential decrease in (offspring) reproductive fitness. Thus, adult birds that are particularly sensitive to the motivational effects of food instability, and enhance their food-seeking behaviors in response, could have more reproductively successful offspring. Therefore, in addition to the natural selection pressure on birds to respond to food unpredictability by increasing food-seeking behavior, there could also be a sexual selection pressure on these birds’ offspring, with potential indirect fitness effects on parental behavior. In theory, the offspring with the best songs after seasons of food shortages – potentially those offspring whose parents were most active in food-seeking behaviors in times of instability – would be favored by sexual selection. Thus, the conceptual framework proposed by A&G has broad relevance to future studies in multiple evolutionary contexts.

The target article explores the causal underpinnings with respect to the direct fitness effects of food unpredictability on the individual level. We suggest that these mechanisms may be complicated when considering the intergenerational fitness effects of clutch rearing, modulated by both offspring sexual selection and survival. Adults tending to nestlings must temporarily dramatically increase their food-seeking behavior; food unpredictability during breeding causes an evolutionary dilemma regarding resource allocation to parents versus offspring. To maximize reproductive success of current offspring, parents should allocate resources overwhelmingly toward nest provisioning; however, depending on the parents’ potential for future breeding success, it may be more advantageous to instead allocate all resources toward self-preservation.

As A&G note, food unpredictability is a known stressor; accordingly, the vast majority of studies on the subject of nest provisioning during harsh conditions have focused on the role of corticosterone, the homolog of human cortisol present in birds. In some avian species, experimentally and endogenously elevated baseline corticosterone levels have been correlated with moderate increases in parental investment, even when they increase the time spent away from the nest, consistent with increased foraging (Bonier et al. Reference Bonier, Moore, Martin and Robertson2009; Reference Bonier, Moore and Robertson2011; Kitaysky et al. Reference Kitaysky, Wingfield and Piatt2001; Miller et al. Reference Miller, Vleck and Otis2009; Ouyang et al. Reference Ouyang, Muturi, Quetting and Hau2013) This may be directly tied to demonstrated inverse relationships between levels of corticosterone and prolactin, the hormone linked to maintaining nest-attendant behavior. Paradoxically, reducing the drive to tend to a brood promotes the requisite departure from the nest to forage.

Any reproductive fitness benefit from elevated corticosterone during food instability, however, seems to have an upper limit, as high levels of corticosterone have resulted in reduced provisioning or complete abandonment of offspring (Kidawa et al. Reference Kidawa, Barcikowski and Palme2017; Silverin Reference Silverin1986). When the threat to survival is severe, it is evolutionarily advantageous for an adult to reallocate all resources away from offspring toward self-preservation. In this situation, corticosterone depresses prolactin enough to overcome nest attachment and facilitate nest abandonment (for a review, see Angelier & Chastel Reference Angelier and Chastel2009).

Very few studies in birds have considered the role of dopamine in modulating reproductive behaviors during periods of food scarcity or in general (Angelier et al. Reference Angelier, Wingfield, Tartu and Chastel2016). Based on evidence from other animal taxa, dopamine may have an important and potentially context-dependent function in mediating foraging behaviors as they relate to reproduction. Studies in rodents have shown that dopamine promotes maternal attachment and that dopamine dysfunction can lead to abandonment of pups (for a review, see Dulac et al. Reference Dulac, O'Connell and Wu2014). We wholly agree with A&G's call for studies testing their predictions regarding dopamine and foraging behaviors in small passerines (sect. 6).

To complement the impressive contributions of the target article, we suggest that, in multiple ways, the discussion of food-seeking behavior is complicated by its link to reproductive success, particularly in passerine birds. Behaviorally, food-seeking behaviors in times of resource uncertainty can have an outsized effect on offspring fitness because the ability to learn song in oscine songbirds is affected by nutritional stress during development, thus linking parental foraging to offspring sexual selection. Extending from the authors’ proposed topics of study, it is worth further investigating the interaction of dopamine and corticosterone and its evolutionary links to songbirds’ foraging-mediated reproductive fitness.