The relationship between parental investment and offspring quality has been investigated in numerous studies that have demonstrated how parents should allocate their investment to maximize their fitness (Temme 1986; Haig 1990; Clutton-Brock 1991; Stearns 1992; Royle et al. 2012). Parents allocate their investment according to factors associated with offspring reproductive value such as mate quality (differential allocation: Burley 1986; Sardell and DuVal 2013), brood size (Coleman et al. 1985; Carlisle 1985), offspring size, age, breeding attempt onset (Winkler 1987), parentage (Westneat and Sherman 1993), offspring sex (Komdeur et al. 1997), and predation risk (Slagsvold 1982; Haight 2018). The allocation of parental investment has been mainly investigated in avian offspring (Slagsvold and Lifjeld 1989; Viñuela 1997; Sardell and DuVal 2013). In birds, the timing of incubation onset is a key event explaining the allocation of parental investment and is a crucial determinant in egg and nestling survival as it realizes asymmetric egg and nestling survivability with respect to egg-laying sequence (Aldredge 2017).
The clutch is completed over several days as female birds cannot lay more than one egg per day (Clark and Wilson 1981). Many birds start incubation before clutch completion in order to shorten the breeding period and reduce the risk of egg or nestling depredation (“nest failure hypothesis”; Clark and Wilson 1981). Alternatively, parents may avoid embryonic death resulting from the failure to incubate eggs that have been laid early (“egg viability hypothesis”; Arnold et al. 1987; Veiga 1992). Incubation onset before clutch completion causes asynchrony in hatching. Late-hatching nestlings incur a competitive disadvantage compared to their early-hatching siblings (Oddie 2000; Bebbington et al. 2017). Therefore, the survival prospect of eggs laid after incubation onset should be negatively correlated with the egg-laying sequence because of this hatching asynchrony. Previous studies have hypothesized that increasing egg size in the laying sequence is a breeding strategy compensating for the disadvantages resulting from hatching asynchrony (Stoleson and Beissinger 1995). In this scenario, female parents increase the size of eggs which are expected to be delayed in hatching in order to increase the body weight of late-hatched nestlings. In other forms, it has been reported as parental compensation, such as an elevation of testosterone level in the yolk to increase the growth of late-hatching nestlings (Schwabl 1993) or preferential provisioning for late-hatching nestlings (Gottlander 1987). Hereafter, this hypothesis is referred to as the “compensatory investment hypothesis” in which parents allocate a comparatively greater investment to eggs or nestlings with poorer survival prospects within the clutch.
On the other hand, the survival of eggs laid before incubation onset should decrease when the egg-laying sequence is early because eggs laid before incubation onset are susceptible to microbial infection (Cook et al. 2005; D’Alba et al. 2010), ambient temperature (Webb 1987), weather conditions (Wang and Beissinger 2009; Coe et al. 2015), and predation or nest site takeover (Clark and Wilson 1981). In these cases, early-hatching nestlings require no compensation for their size. Instead, female parents may allocate investment in egg size according to survival prospects of the eggs laid before incubation onset. Declining egg size over the laying sequence in some birds (Poole 1982; Meathrel and Ryder 1987; Svagelj et al. 2015; Djerdali et al. 2016) is explained by unpredictable breeding environments (“brood reduction hypothesis”; Lack 1947; Slagsvold et al. 1984). This hypothesis proposes that late-hatching nestlings are surplus and survive only when there is a lot of food available for the parents to feed their nestlings. Unlike the aforementioned “compensatory investment hypothesis”, this theory (the “proportional investment hypothesis”) suggests that parents should allocate comparatively less investment to eggs or nestlings with lower survival prospects within the clutch.
Collectively, there are two different investment strategies in egg and nestling size. As mentioned, the timing of the onset of incubation is a crucial determinant in the survival prospects of the eggs and nestlings. Therefore, birds that initiate incubation before clutch completion could adopt both (different) investment strategies in a breeding attempt. However, this possibility has never been tested.
We conducted an observational study to test the hypothesis that the survival prospects of the eggs are highest for eggs laid on the day of incubation onset in the wryneck Jynx torquilla, an altricial Piciformes species. The wryneck is migratory bird, and it returned to our study site in April. Wrynecks nest in a cavity and are social monogamous. Both sexes incubate eggs and provide foods for nestlings. We investigated the relationships among incubation onset, egg volume, egg viability, hatching asynchrony, nestling growth, and fledging success. We predicted that the viability of eggs laid before incubation onset until hatching would increase with a decrease of temporal distance (the number of days between laying and the day of incubation onset within the clutch), but the viability of eggs laid after incubation onset until hatching would be constant, irrespective of temporal distance (Prediction 1, Fig. 1a). Contrary to these, we predicted that the survival of nestlings hatched from eggs laid before incubation onset until fledging would be constant, irrespective of temporal distance, but the survival of nestlings hatched from eggs laid after incubation onset until fledging would decrease with an increase of temporal distance (Prediction 2, Fig. 1b).
If the survival of eggs laid before incubation onset decreases (Prediction 1) and the survival of nestlings hatched from eggs laid after incubation onset decreases (Prediction 2), the viability of eggs from laying to fledging would be highest for eggs laid on the day of incubation onset (Fig. 1c). In this case, when female parents only adopt proportional investment through egg laying, egg size and egg viability until fledging should show a positive correlation (Fig. 2a: the size of eggs laid before incubation onset should increase with decreasing temporal distance, and the size of eggs laid after incubation onset should decrease with increasing temporal distance). Contrary to this, when female parents only adopt compensatory investment, egg size and egg viability until fledging should show a negative correlation (Fig. 2b: the size of eggs laid before incubation onset should decrease with increasing temporal distance, and the size of eggs laid after incubation onset should increase with decreasing temporal distance). If female parents adopt different investment strategies for eggs laid before and after the onset of incubation, egg size should show mixed patterns (Fig. 2c, d). Female parents may perform proportionate investments in egg volume before incubation onset because early-hatching nestlings require no compensation for their size. On the other hand, eggs laid after the onset of incubation require compensation for their size as this characteristic is positively associated with nestling body mass (Williams 1994; Styrsky et al. 1999). In this way, late-hatching nestlings can contend with sibling competition. Here, we predict that egg size should increase with decreasing temporal distance before incubation onset by proportional investment, and egg size should also increase with increasing temporal distance before incubation onset by compensatory investment (Prediction 3, Fig. 2c).
Furthermore, as the compensatory investment hypothesis predicts that female parents should produce comparatively larger eggs after the onset of incubation, there should be different growth patterns between the early- and late-hatching nestlings within the same clutch. We predicted that late-hatching nestlings will grow faster than early-hatching nestlings (Prediction 4) when the compensatory investment hypothesis is upheld.