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Interactions within the family are regulated by both cooperation and conflict. Whilst parents cooperate with each other to rear offspring, and provide care to their offspring at a cost to themselves, conflict arises between family members over the amount of care to be provided (Trivers, 1972, 1974).

Notably, sexual conflict over parental care, as first formulated by Trivers (1972), occurs when parents share equally the benefit of caring (through increased offspring fitness), but only pay the cost of their own investment in parental care. To maximise its benefit-to-cost ratio, a parent should therefore decrease its own effort and let its partner compensate for the shortfall (Trivers, 1972). Theory generally predicts that, in order for bi-parental care to be evolutionary stable, individuals should only partially compensate for their partner's shortfall (Houston and Davies, 1985; McNamara et al., 1999). Whilst most empirical studies conform to this prediction, many others find full compensation, no change, or instead a decrease in investment as individuals match their partner's effort (reviewed in Hinde, 2006; Harrison et al., 2009). Theory predicts that some of this variation may arise from partners' disparity in access to information about offspring needs, if the least informed parent cues on its partner, thereby matching its effort (Johnstone and Hinde, 2006; Hinde and Kilner, 2007).

Mariette and Griffith (2012, 2015) further proposed that the coordination of parental care could not only lead to investment matching, but may also improve parental care efficiency. Indeed, even though theoretical models generally assume otherwise (but see Johnstone and Savage, 2019), partners may partly share the cost of parental care when it impairs their continued investment within the current breeding attempt or in following attempts with the same partner (Mariette and Griffith, 2015). If so, optimising provisioning may prevail over exploiting partner's efforts, and it is expected that, by providing a simple reciprocity rule, coordination may facilitate negotiation and decrease the cost of sexual conflict (Johnstone et al., 2014). Accordingly, we showed that wild zebra finch parents (Taeniopygia guttata) synchronise provisioning by visiting the nest together during nestling rearing, and that better coordinated pairs produce more fledglings (Mariette and Griffith, 2012). Furthermore, consistent with an efficiency benefit of coordination, partners increased nest visit synchrony when parental workload (brood size) was experimentally increased, and nestling condition increased with parental coordination during foraging (Mariette and Griffith, 2015). Interestingly, we also showed that acoustic communication plays a central role in breeding partners interactions at the nest (Elie et al., 2010), including for the coordination of parental care (Boucaud et al., 2016a, 2017). Likewise, parental care coordination, either by alternating or synchronising nest visits, has been evidenced in several other avian species (e.g., Raihani et al., 2010; Bebbington and Hatchwell, 2016; Koenig and Walters, 2016; Savage et al., 2017; but see Khwaja et al., 2017), including in bi-parental care species with short-term pair bonds (Johnstone et al., 2014; Lejeune et al., 2019) and complex acoustic communication between partners (Gorissen and Eens, 2005). Although the effect on nestling growth is largely unknown (but see Iserbyt et al., 2017; Wojczulanis-Jakubas et al., 2018) and varies with ecological conditions (Lejeune et al., 2019) and foraging behaviour (Mariette and Griffith, 2015), the accumulation of recent studies clearly show that parental care coordination and equitable negotiation are more common than previously assumed.

Here, I further show how multiple other aspects of cooperation have been overlooked, by failing to consider the communication between family members, and the information it conveys. For example, there is some evidence in birds that skin or bill colour signals individual condition, which parents may cue on to adjust their reproductive investment relative to their partner's current provisioning capacity or offspring needs (e.g., foot colour in blue-footed boobies: Velando et al., 2006; Dentressangle et al., 2008; nestling mouth coloration: Ewen et al., 2008). However, even though visual and chemical signals are used, acoustic signals are likely to play a particularly prominent role in avian family communication. Indeed, acoustic signals can readily indicate individuals' immediate state and perhaps their short-term intentions. In addition, interactive acoustic communication, whereby individuals adjust their vocalisations in response to others' signalling, is especially well-suited for real-time negotiation (e.g., Ducouret et al., 2019). Lastly, unlike other senses, the acoustic (or vibratory) channel allows a sophisticated level of communication and negotiation to occur prenatally, in parent-embryo and embryo-embryo interactions (Mariette and Buchanan, 2019b; Noguera and Velando, 2019).

Surprisingly however, with the notable exception of nestling begging calls, the importance of acoustic communication for cooperation within the family has received very little attention. Here, I highlight the role of acoustic communication between breeding partners in parental care coordination. I then point to the multiple ways in which acoustic communication may alter parent-offspring cooperation and co-adaptation, before and after birth. Lastly, I discuss the role of begging calls and other offspring vocalisations in sib-sib interactions, including prenatally.

The hypothesis that acoustic communication allows partners to negotiate their relative efforts in real-time was first proposed by Boucaud et al. (2016a) (Figure 1). In this study on captive zebra finches, where both partners incubate, we experimentally delayed the return to the nest of the male partner during incubation, and recorded vocal interactions at the nest. As predicted, partners' acoustic interactions were altered by the male delay. More strikingly however, the time the female subsequently stayed off the nest was predicted by her partner's calling rate when he returned, rather than by how long she had been incubating for. Likewise, the female's calling rate when her belated mate returned was the best predictor of the duration of her next incubation bout (Boucaud et al., 2016a). This suggests the male also cued on its partner's vocal behaviour rather than on the female's recent investment, although the reciprocal experiment (delaying female's return) would be interesting to carry. Overall, it therefore appears that individuals signal their need to be off the nest by calling more during nest reliefs, and that the partner respond to this signal by coming back early to relieve its partner. Acoustic communication may thus inform individuals on their partner's state, and hence on the cost of a prolonged incubation bout in that particular moment. Having access to such information, partners may not simply match their investment (i.e., time spent incubating), but instead match the cost of that parental care investment (e.g., as in Griffioen et al., 2019). If so, focussing research on the matching of investments rather than on their costs may misrepresent individuals' investment decisions, and importantly underestimate the level of cooperation within pairs (see also, asymetries in “recovery rate” in Johnstone and Savage, 2019).

In follow up studies, Boucaud, Vignal, and collaborators further demonstrated that females may signal their immediate needs to their partner by vocalizing from inside the nest when the male arrives in the vicinity (Boucaud et al., 2016c, 2017). In wild zebra finches, female calling rate and her calls' acoustic structure on her mate arrival predicted whether or not the male relieved the female for incubation (Boucaud et al., 2017). Likewise, in wild great tits (Parus major), with female-only incubation, female's vocalisations, and the pair's vocal interactions differed depending on whether or not the male entered the nest to feed the female (Gorissen and Eens, 2005; Boucaud et al., 2016c). Moreover, when great tit females were experimentally supplemented with food, they altered their vocalisations, uttered before and after the male entered the nest (Boucaud et al., 2016b). This suggests that female vocalisations may honestly signal her needs, and that the male potentially receives information on female's state even from outside the nest. What would appear as a male-only decision (whether or not to relieve/feed the female) when acoustic information is ignored, may in fact be a negotiated decision, incorporating the female's needs. These studies again reveal a higher level of cooperation between partners than is generally assumed, including in species with short-term pair-bonds.

By far the most studied aspect of acoustic communication within the family is offspring begging calls and their importance for parent-offspring negotiation and conflict mitigation (reviewed in Kilner and Johnstone, 1997; Royle et al., 2002; Kilner and Hinde, 2012). Parent-offspring conflict arises because offspring's provisioning rate optimum is expected to be higher than that of their parents, who trade-off current with future reproductive investment, as well as offspring quality with quantity (Trivers, 1974; Stearns, 1992; Kilner and Hinde, 2012). Yet, the costs of begging on the offspring maintain begging as an honest signal of needs, that parents may cue on (Kilner and Johnstone, 1997; Kilner, 2001). Moreover, begging sensitivity to maternal hormones provides a mechanism for mothers to control their offspring's begging display (Eising et al., 2001), potentially allowing the co-adaptation of begging display and parental provisioning capacity (Hinde et al., 2009, 2010). It is clear from this large body of work that considering information transfer through acoustic signals can drastically alter our understanding of conflict and cooperation within the family.

Beside offspring vocalisations, parents are also known to communicate vocally with their nestlings, particularly using alarm or food calls (Madden et al., 2005; Magrath et al., 2007 and references therein). These parental vocalisations have been hypothesised to reduce detection of nests by predators cueing on loud nestling begging calls. Specifically, parental alarm calls for nest predators are found to supress begging (Madden et al., 2005; Platzen and Magrath, 2005), whereas in some species, parents produce food calls when arriving at the nest, which generally indicates to nestlings that it is safe to beg (Madden et al., 2005; Magrath et al., 2007). Indeed, whilst fledglings may blackmail parents by begging in dangerous locations (Thompson et al., 2013), we may expect parents and nestlings to cooperate more closely, as both equally benefit from avoiding detection by predators when nestlings are not yet mobile.

Even though negotiation has been identified as a key process for the evolution of cooperation and parental care (McNamara et al., 1999, 2003; Johnstone and Hinde, 2006), we know surprisingly little on how negotiation operates, particularly on a behavioural time scale. The evidence brought together here strongly suggests that acoustic communication is likely to play a central role in family negotiation and cooperation. Interestingly, the evidence above on vocal negotiation between incubating partners, temperature-dependent calls in both parents or embryos, and vocal cooperation between siblings pre and post-natally, consistently demonstrates that considering acoustic communication often reveals previously unsuspected cooperative interactions where conflict had instead been considered as the driving force. This likely stems from the capacity of acoustic signals to convey large amount of information, notably on individual's hunger or thermal state in both parents and offspring. Access to this information can drastically alter investment decisions, by allowing the optimisations of costs and benefits to family members. A theoretical approach will be highly valuable in predicting the impact of prenatal and postnatal acoustic communication on the evolution of cooperation and parental care.

In addition, more empirical studies are clearly needed on a range of species to understand the generality of the patterns highlighted here. Beside their ubiquity in many taxa, acoustic signals are particularly amenable to fine experimental research using playbacks and continuous recordings, including automatic interactive playbacks (Ducouret et al., 2019) and playbacks targeting specific individuals (e.g., Hinde and Kilner, 2007). Integrating acoustic communication to the study of cooperation is therefore a highly promising field of research.

MM conceived the manuscript, reviewed published literature, and wrote the manuscript.