Species divergence in offspring begging and parental provisioning is linked to nutritional dependency

Species divergence in offspring begging and parental provisioning is linked to nutritional... Abstract In animal species in which parents provide food to their dependent young, offspring often display conspicuous begging signals. These solicitation behaviors are important components of parent–offspring communication, but it is currently unclear how they and the parental response covary with offspring dependency on parental food provisioning across species. Burying beetles (Nicrophorus) are well known for providing elaborate biparental care, including provisioning of begging larvae. By using a multispecies approach, we show that larval begging intensity, as well as the time parents spend provisioning, differ greatly between individuals of the 3 species: N. orbicollis, N. pustulatus, and N. vespilloides. Our results demonstrate that the most dependent offspring of N. orbicollis invest the most time in begging, whereas the most independent offspring of N. pustulatus invest the least amount of time in begging. Thus, we suggest that begging intensity differs due to intrinsic differences in nutritional need between the species rather than because of an arbitrary divergence in begging behavior. We further show that in all 3 species, females spend significantly more time provisioning than males, although there is considerable divergence between species in the extent to which females and males contribute to the provisioning of larvae. We discuss the potential selective factors leading to this diversification of offspring begging and parental provisioning in relation to the distinct variation in offspring dependence between the 3 species. INTRODUCTION Communication between parents and offspring plays an essential role in animal species in which parents provide care to increase their offspring’s fitness (Clutton-Brock 1991). One important component of parent–offspring communication involves elaborate acoustic, visual, chemical, or tactile begging signals of offspring to solicit resources from caring parents (Kilner and Johnstone 1997). Such begging displays are supposed to reflect short-term need (i.e., hunger) of offspring that parents use to adjust their food allocation (e.g., Mock et al. 2011). Evidence for intense interactions between parental provisioning and offspring begging mainly comes from studies on birds or mammals (Kilner and Johnstone 1997). In several bird species, for example, food-deprived chicks have been shown to beg more intensively than well-fed chicks to advertise their hunger level to caring parents (e.g., Mondloch 1995; Price and Ydenberg 1995). However, the intensity of begging may also depend on the total amount of food required prior to independence, which is often referred to as the long-term need (Price et al. 1996). Given the same feeding rate and amount, offspring with an overall higher long-term need are expected to beg more intensively. In fact, evidence in support of this proposition comes from a study on yellow headed blackbirds (Price et al. 1996). As begging should influence offspring growth and survival, and the magnitude of this effect in turn depends on how dependent the offspring are on their parents’ food (i.e., the overall fitness benefit of receiving parental food), the degree of offspring dependency must be considered to understand the evolutionary interplay between begging signals and parental response to these signals. We would, for example, predict offspring to vary in their intensity of begging according to how dependent they are on parental provisioning, both within and between species. There are, however, few studies that have explored the divergence in begging behavior between different species. In a partial cross-fostering experiment, Qvarnström et al. (2007) found that young of pied and collared flycatchers (Ficedula hypoleuca and Ficedula albicollis) showed a strong difference in their begging intensity, suggesting that the observed difference in begging intensity reflects a genetic difference in offspring need to which the parents of both species respond. Although this latter study certainly demonstrates between-species variation in begging intensity, it does not allow any conclusions about how begging behavior covaries with how dependent the offspring are on parental provisioning. From a behavioral and evolutionary viewpoint, it is important to consider offspring begging together with the parental response to begging, that is, the amount of food provided. As parental provisioning and offspring begging reciprocally influence each other, both traits are expected to coevolve and may become genetically correlated, ultimately leading to coadaptation of parental and offspring traits (Wolf and Brodie 1998; Kölliker et al. 2005; Meunier and Kölliker 2012). As the coevolution of supply (parental provisioning) and demand (offspring begging) can generate a positive or a negative correlation between parent and offspring traits, depending on whether parents or offspring are in control of food allocation (Kölliker et al. 2005; Smiseth et al. 2008; Hinde et al. 2010), the outcome of this coevolution might differ. The coevolutionary trajectory of provisioning and begging intensity might diverge between species according to genetic differences in need or arbitrarily due to differences in the escalation of parent–offspring conflict. Thus, to investigate the early evolution of provisioning and begging, a multispecies approach, involving different species that vary in the ability of offspring to self-feed and their concomitant reliance on parental provisioning, could be highly informative. Furthermore, greater offspring demand might select for higher provisioning rates in both parents, or, alternatively, only one of the sexes might be targeted. In general, it is important to consider that the evolutionary interests of male and female parents over parental investment often do not coincide (Trivers 1972). Consequently, sex differences in food provisioning may arise and one sex might be more responsive to offspring begging than the other. Across diverse animal taxa, females are known to provide more care than males, and there is evidence from birds, mammals and insects that males and females differ in their response to offspring begging (Kölliker et al. 1998; Kilner 2002; Quillfeldt et al. 2004; Smiseth and Moore 2004a; English et al. 2008). Nevertheless, the degree of sex differences in offspring provisioning might vary across closely related species, that is, there might be species in which both parents are nearly equally responsive to offspring begging, whereas in others, one of the sexes might do the majority of the work. Differences between males and females in the decision rules regarding parental provisioning could greatly influence the fitness of dependent offspring, and thus it could be fruitful to examine whether such sex differences in parental provisioning vary across species. Burying beetles of the genus Nicrophorus are well known for exploiting small vertebrate carcasses and providing extensive biparental care to their offspring including regurgitation of carrion (Pukowski 1933; Eggert and Müller 1997; Eggert et al. 1998; Scott 1998). Larvae can feed independently, but also beg for predigested food by raising their head toward the parent while waving their legs or touching the parent with their legs (Rauter and Moore 1999; Smiseth et al. 2003). Previous studies on burying beetles have found that begging reflects an offspring’s hunger level (Smiseth and Moore 2004b), and that larvae adjust the time spent begging according to brood size and behavior of competing siblings and caring parents (Rauter and Moore 1999; Smiseth and Moore 2002), as well as their proficiency at self-feeding (Smiseth et al. 2003). Larvae have also been shown to beg only when a parent is nearby (Rauter and Moore 1999; Smiseth and Moore 2002). In turn, parents respond to begging by adjusting the time spent allocating resources to offspring (Smiseth and Moore 2002, 2008). We recently showed that offspring of 3 species, N. orbicollis, N. pustulatus, and N. vespilloides, show striking variation in their reliance on parental care (Capodeanu-Nägler et al. 2016). In that study, we manipulated the occurrence of prehatching (no care or care) and/or posthatching care (no care or care) in each of the 3 species and found a differential reliance on posthatching care, which consists mainly of food provisioning, but not on the prehatching component of parental care. In the majority of cases, none of the larval N. orbicollis survived in the absence of parental feeding, indicating obligate parental care in this species. In contrast, in N. pustulatus, larval survival and growth was not reduced in the absence of parents. The reliance of N. vespilloides larvae on posthatching care appears to be intermediate, as offspring survival and growth in the absence of posthatching care was better than in N. orbicollis, but worse than in N. pustulatus. Consequently, these results indicate that there are contrasting nutritional requirements, and that the fitness benefits of food provisioning differ between the offspring of the 3 species. In the present multispecies study, we tested the hypothesis that offspring of the 3 Nicrophorus species vary in their amount of begging and that parents, in turn, have adapted to respond to this variation by modulating the amount of food provided. If begging intensity of larvae is related to the degree of offspring dependence and the offspring’s need for nutritional resources, we further predicted that larvae of N. orbicollis, which show the strongest reliance on parental care, would also display the strongest begging behavior to solicit more food from their parents. In contrast, N. pustulatus offspring that appear to be nutritionally independent of their parents are predicted to beg less and to be fed the least by their parents. We predicted that N. vespilloides, in which larvae are only partially dependent on parental provisioning, would show an intermediate amount of begging and provisioning behavior. We additionally tested for sex differences in the time spent provisioning the larvae, as previous studies have shown that females spend more time feeding the larvae than males (Fetherston et al. 1990, 1994; Rauter and Moore 1999, 2004; Smiseth and Moore 2004b). MATERIALS AND METHODS Origin and maintenance of experimental animals Experimental N. vespilloides were descendants of beetles collected from carrion-baited pitfall traps in a forest near Ulm, Germany (48°25′03′′N, 9°57′45′′E). Cultures of N. pustulatus and N. orbicollis were established at Ulm University from outbred colonies maintained at the Institute of Zoology, University of Freiburg, Germany. We maintained outbred colonies of both species by introducing beetles captured in baited pitfall traps established in a forested area near Lexington, IL (40°39′57′′N, 88°53′49′′W). All beetles were maintained in temperature-controlled chambers at 20 °C on a 16:8 h light:dark cycle. Before the experiments, groups of up to 5 adults of the same sex and family of each species were kept in small plastic containers (10 × 10 cm and 6 cm high) filled with moist peat. Beetles were fed freshly decapitated mealworms ad libitum twice a week. At the time of experiments, beetles were virgin and between 30 and 40 days of age. Experimental design For our study, nonsibling pairs of beetles were randomly paired and reproduction was induced by providing them with a 20 g (± 3 g) thawed mouse carcass (Frostfutter.de—B.A.F Group GmbH, Germany). In the case of the nocturnal species, N. pustulatus and N. orbicollis, mice were provided during the dark portion of the photoperiod. After the egg-laying period, but before larvae hatched (see Capodeanu-Nägler et al. 2016), parents and the carcass were transferred to new plastic containers filled with soil. The eggs were left to hatch in the old container, which we checked every 8 h for the presence of newly hatched larvae. We weighed the larvae when they hatched (0 h), before providing each pair of beetles with a brood of 15 newly hatched larvae of mixed parentage to control for variation between families and individual differences in behavior (Rauter and Moore 1999). As brood size is known to affect larval begging (Smiseth and Moore 2002; Smiseth et al. 2007) as well as parental provisioning (Rauter and Moore 1999; but see Smiseth and Moore 2002), we opted for a standardized brood size of 15 larvae. The larvae were placed directly onto the carcass, which we had sliced open earlier to facilitate their access to the carrion. As females exhibit temporally-based kin discrimination in which they kill any larvae arriving on the carcass before their own eggs would have hatched, but accept larvae that arrive after their own eggs have begun to hatch (Müller and Eggert 1990), we provided pairs with larvae only after their own larvae had begun hatching. We established broods until attaining a minimum sample size of 15 for each species (n = 20 for N. orbicollis, n = 20 for N. pustulatus, n = 15 for N. vespilloides). We conducted behavioral observations on larval begging and parental food provisioning at 24 and 48 h, respectively, when larvae have reached the second instar and larval begging is known to peak (Smiseth and Moore 2002; Smiseth et al. 2003). We used instantaneous scan sampling every 1 min for 30 min (Martin and Bateson 1986) to record larval and parental behavior (Rauter and Moore 1999). To facilitate discrimination between the sexes, we marked males with a dot of white correction fluid on one elytron and a dot on the pronotum (Rauter and Moore 2002). At each scan, we recorded the following traits and behaviors: 1) The number of larvae that were begging. A larva was considered to be begging when it raised its head towards the parent while waving its legs, or touched the parent with its legs (Rauter and Moore 1999; Smiseth and Moore 2002). 2) The number of mouth-to-mouth contacts between a parent and at least one larva, indicating parental provisioning. 3) The sex of the parent providing food to the larvae. 4) The proximity of parents to the larvae, defined as the distance less than the width of the parent’s pronotum from the larvae, as larvae begin begging only when a parent is close by (Rauter and Moore 1999; Smiseth and Moore 2002). Before beginning observations, we covered each box containing parents, larvae and the carcass with a thin glass panel (12 × 12 cm), allowing individuals to acclimatize for 15 min. We weighed the larvae of each brood at 2 additional time points, at the end of the 48-h observation period, and upon their dispersal from the carcass. Statistics All data were analyzed and plotted using R version 3.1.2 (R Core Team 2014). For larval begging behavior, we calculated the average percentage of time spent begging by larvae in each brood, bi, as bi = ∑b/L × 100/30, where b is the total number of larval begging events during the 30 scans of an observation session, and L is the brood size (Smiseth and Moore 2002, 2004b), which in our experiments always corresponded to a brood size of 15 larvae. As larvae beg only when parents are close by, we also calculated the average percentage of larval begging time in the presence of parents as a second parameter (Smiseth and Moore 2004b). For this metric, we replaced the total number of 30 observation scans in the formula with the number of scans when at least one of the parents was in close proximity to the larvae. For calculating parental food provisioning, we used the same formula as for larval begging behavior, replacing the total number of begging events bi with the total number of mouth-to-mouth-contacts for all 30 scans, as well as for all scans when at least one of the parents was in close proximity. By using the lmer function from the lme4 package, we then performed linear mixed-effect models (LMMs) in which we included brood ID as a random factor to control for repeated measurements in our design. We used species, the time of observation and species × time of observation as fixed factors, and the average percentage of larval begging time during all observations (30 scans), the average percentage of larval begging time when parents were in close proximity, the average percentage of parental food provisioning during all observations, and the average percentage of parental food provisioning when parents were in close proximity as dependent variables. To localize species-specific differences, we then continued with simpler generalized linear models (GLMs) followed by post-hoc Tukey comparisons in which species was included as a fixed factor with the same dependent variables as described above. Within species, we also performed GLMs in which we included the sex of the provisioning parent, time of observation, and the interaction between sex and time as fixed factors, and each of the parameters measuring parental food provisioning as dependent variables. In addition, we performed GLMs within species with the time of observation as a fixed factor, and both parameters measuring begging behavior as dependent variables. Further, we calculated the proportion of time that parents stayed in close proximity to the larvae relative to the total number of all observation scans by creating a 2-column response vector consisting of the number of positives (i.e., parents in close proximity) and the number of negatives (parents not in close proximity) joined together by the function cbind. We then applied GLMs with a quasi-binomial distribution. The same statistical approach was used to compare larval survival (i.e., larvae survived vs. larvae not survived) at dispersal. We compared the mean larval mass per brood of the species at different points in development (0 h, 48 h, and upon dispersal of the larvae), and the time until larval dispersal by using GLMs with a Gaussian distribution. RESULTS Larval begging behavior We found significant effects of species and the time of observation as well as an interaction of both effects on larval begging behavior (Table 1). When parents were in close proximity to larvae, begging behavior differed significantly between larvae of all 3 species (Table 1; Figure 1). Larvae of N. orbicollis spent more time begging than larvae of N. pustulatus (Tukey’s post-hoc test: P < 0.001) and N. vespilloides (Tukey’s post-hoc test: P = 0.01). In addition, N. vespilloides larvae spent more time begging than N. pustulatus larvae (Tukey’s post hoc test: P < 0.001). With respect to all scans during an observation session irrespective of parental proximity, begging behavior still significantly differed between larvae of the 3 species (Table 1; Supplementary Figure S1). However, post-hoc comparisons showed that there was no longer a significant difference between the time invested in begging by N. orbicollis and N. vespilloides larvae (Tukey’s post-hoc test: P = 0.19). Table 1 Results of LMMs of the effect of species (N. orbicollis, N. pustulatus, N. vespilloides), time of observation (24 h or 48 h), and the interaction of species and time of observation on larval begging for scans when parents were in close proximity and for the whole observation period   Begging parent/s present  Begging all observation scans  Factor  X2  P  X2  P  Species  88.01  <0.001  58.99  <0.001  Time of observation  12.26  <0.001  7.70  0.006  Species × time of observation  8.52  0.014  12.96  0.002    Begging parent/s present  Begging all observation scans  Factor  X2  P  X2  P  Species  88.01  <0.001  58.99  <0.001  Time of observation  12.26  <0.001  7.70  0.006  Species × time of observation  8.52  0.014  12.96  0.002  Significant P values are typed in bold. View Large Figure 1 View largeDownload slide The time spent begging by each larva (%) when parents were in close proximity at 24 h and 48 h. Boxplots show median, interquartile range, minimum/maximum range. The dots are values that fall outside the interquartile range (>1.5 × interquartile range). Figure 1 View largeDownload slide The time spent begging by each larva (%) when parents were in close proximity at 24 h and 48 h. Boxplots show median, interquartile range, minimum/maximum range. The dots are values that fall outside the interquartile range (>1.5 × interquartile range). Time of observation (24 h or 48 h) had an effect on begging, but this effect differed between the species (Table 1). For both begging parameters, we found that N. vespilloides and N. orbicollis larvae reduce begging from 24 h to 48 h, whereas larval N. pustulatus tend to increase begging. To better understand how time affects begging, we analyzed the species separately. In N. orbicollis and N. pustulatus, the time of observation had no effect on the average time larvae spent begging, regardless of whether all scans in an observation session were included (GLM with Gaussian errors: F1,38 = 0.29, P = 0.59 for N. orbicollis; F1,38 = 0.17, P = 0.68 for N. pustulatus) or only those scans when at least one parent was in close proximity (GLM with Gaussian errors: F1,38 = 3.27, P = 0.08 for N. orbicollis; F1,38 = 0.02, P = 0.89 for N. pustulatus, Supplementary Figure S2). Also, in both species, there was no significant correlation between the time invested in begging at 24 h and the time invested in begging at 48 h, both when all observation scans were considered (Pearson correlation: r = 0.36, n = 40, P = 0.12 for N. orbicollis; r = 0.09, n = 40, P = 0.71 for N. pustulatus) and when only those scans when parents were close by were included (Pearson correlation: r = 0.25, n = 40, P = 0.28 for N. orbicollis; r = 0.09, n = 40, P = 0.70 for N. pustulatus). In N. vespilloides, we found that the same brood that invested a lot of time in begging at 24 h also invested more time at 48 h, whereas broods that invested less time in begging at 24 h also invested less time at 48 h. This was true for all observation scans (Pearson correlation: r = 0.58, n = 30, P = 0.02), as well as for the scans in which parents were in close proximity (Pearson correlation: r = 0.53, n = 30, P = 0.04, Supplementary Figure S2). For both begging parameters, the time of observation had a negative effect on larval begging behavior in N. vespilloides (GLM with Gaussian errors: F1,28 = 14.26, P < 0.001 for all observation scans; F1,28 = 12.28, P = 0.002 for scans with parents present only). On average, larvae reduced begging, that is, they begged at lower intensities at 48 h than after 24 h of development. Parental food provisioning We found that species but not the time of observation significantly affected parental food provisioning (Table 2). Furthermore, the interaction between species and time of observation had a significant effect on parental provisioning (Table 2). Food provisioning from parents to larvae differed significantly between the 3 species, regardless of whether we included all scans of an observation session (Table 2; Supplementary Figure S3) or only those scans in which parents were in close proximity to larvae (Table 2; Figure 2). Parents of N. pustulatus invested the least amount of time feeding their larvae. There was no difference in the time spent provisioning between parents of N. orbicollis and parents of N. vespilloides (Tukey’s post-hoc test: P = 0.96 for all observation scans; P = 0.55 for scans with parents present only). Table 2 Results of LMMs of the effect of species (N. orbicollis, N. pustulatus, N. vespilloides) and the time of observation (24 h or 48 h) and the interaction of factors on parental feeding to larvae for scans when parents were in close proximity and for the whole observation period   Feeding parent/s present  Feeding all observation scans  Factor  X2  P  X2  P  Species  47.90  <0.001  43.55  <0.001  Time of observation  1.91  0.167  1.53  0.216  Species × time of observation  10.03  0.007  21.69  <0.001    Feeding parent/s present  Feeding all observation scans  Factor  X2  P  X2  P  Species  47.90  <0.001  43.55  <0.001  Time of observation  1.91  0.167  1.53  0.216  Species × time of observation  10.03  0.007  21.69  <0.001  Significant P values are typed in bold. View Large Figure 2 View largeDownload slide The time parents spent provisioning larvae (%) for scans when parents were in close proximity at 24 h and 48 h. Boxplots show median, interquartile range, minimum/maximum range. The dots are values that fall outside the interquartile range (>1.5 × interquartile range). Figure 2 View largeDownload slide The time parents spent provisioning larvae (%) for scans when parents were in close proximity at 24 h and 48 h. Boxplots show median, interquartile range, minimum/maximum range. The dots are values that fall outside the interquartile range (>1.5 × interquartile range). Time of observation (24 h or 48 h) had an effect on parental provisioning, but this effect differed between the species (Table 2). Parental provisioning did not change with offspring age in N. orbicollis, whereas it clearly decreased in N. vespilloides and tended to increase in N. pustulatus. To better understand how time affects parental provisioning, we analyzed the species separately. In N. orbicollis and N. pustulatus, the time of observation had no effect on the average time parents spent provisioning, regardless of whether we included all scans of an observation session (GLM with Gaussian errors: F1,58 = 0.20, P = 0.65 for N. orbicollis; F1,32 = 0.84, P = 0.37 for N. pustulatus), or the subset of scans when at least one parent was close by (GLM with Gaussian errors: F1,58 = 2.05, P = 0.16 for N. orbicollis; F1,32 = 0.37, P = 0.55 for N. pustulatus; Supplementary Figure S5). There was no significant correlation between the time invested in provisioning at 24 h and the time invested in provisioning at 48 h in either species, both when all observation scans were considered (Pearson correlation: r = 0.36, n = 40, P = 0.12 for N. orbicollis; r = 0.09, n = 40, P = 0.71 for N. pustulatus) and in the subset of scans when parents were close by (Pearson correlation: r = 0.25, n = 40, P = 0.28 for N. orbicollis; r = 0.09, n = 40, P = 0.70 for N. pustulatus). In N. vespilloides, parents spent significantly more time provisioning at 24 h than at 48 h, both when all observation scans are considered (GLM with Gaussian errors: F1,54 = 12.58, P < 0.001), and in the subset of scans when parents were in close proximity (GLM with Gaussian errors: F1,54 = 9.72, P = 0.003; Supplementary Figure S5). However, for both provisioning parameters, there was no correlation between the time a N. vespilloides parent invested in provisioning at 24 h and the time it invested in provisioning at 48 h (Pearson correlation: r = 0.50, n = 30, P = 0.06 for all observation scans; r = 0.37, n = 30, P = 0.18 for scans with parents present only). This is also true if we consider females (Pearson correlation: r = 0.29, n = 15, P = 0.30 for all observation scans; r = 0.42, n = 15, P = 0.12 for scans with parents present only) and males separately (Pearson correlation: r = −0.09, n = 15, P = 0.74 for all observation scans; r = −0.03, n = 15, P = 0.92 for scans with parents present only). The interaction between the sex of the provisioning parent and the time of observation was not statistically significant, regardless of whether we included all scans of an observation session (GLM with Gaussian errors: F1,58 = 0.04, P = 0.84 for N. orbicollis; F1,32 = 1.06, P = 0.31 for N. pustulatus; F1,54 = 1.57, P = 0.22 for N. vespilloides) or the subset of scans in which parents were in close proximity to larvae (GLM with Gaussian errors: F1,58 = 3.11, P = 0.08 for N. orbicollis; F1,32 = 0.51, P = 0.48 for N. pustulatus; F1,54 = 0.33, P = 0.57 for N. vespilloides). Within each of the 3 species, the female parent spent significantly more time provisioning larvae than the male parent. This was true when all scans in an observation session were included (GLM with Gaussian errors: F1,58 = 77.49, P < 0.001 for N. orbicollis; F1,32 = 23.52, P < 0.001 for N. pustulatus; F1,54 = 13.78, P = 0.001 for N. vespilloides, Supplementary Figure S4), and in the subset of scans when at least one of the parents was close by (GLM with Gaussian errors: F1,58 = 125.00, P < 0.001 for N. orbicollis; F1,32 = 21.52, P < 0.001 for N. pustulatus; F1,54 = 18.38, P < 0.001 for N. vespilloides, Figure 3). Interestingly, we found interspecific differences in the time spent provisioning when analyzing each sex independently (GLM with Gaussian errors: F2,75 = 6.65, P = 0.002 for males; F2,75 = 23.10, P < 0.001 for females). For scans in which parents were in close proximity, male N. vespilloides provided significantly more food than male N. orbicollis (Tukey’s post-hoc test: P = 0.03) and male N. pustulatus (Tukey’s post-hoc test: P = 0.001). In contrast, female N. orbicollis spent significantly more time provisioning than female N. pustulatus (Tukey’s post-hoc test: P < 0.001) and female N. vespilloides (Tukey’s post-hoc test: P < 0.001). We also found that female N. vespilloides spent more time feeding than female N. pustulatus when analyzing all observation scans (Tukey’s post-hoc test: P = 0.02). Figure 3 View largeDownload slide Sex differences in the time spent provisioning the larvae (%) for scans when parents were in close proximity. Boxplots show median, interquartile range, minimum/maximum range. The dots are values that fall outside the interquartile range (>1.5 × interquartile range). Figure 3 View largeDownload slide Sex differences in the time spent provisioning the larvae (%) for scans when parents were in close proximity. Boxplots show median, interquartile range, minimum/maximum range. The dots are values that fall outside the interquartile range (>1.5 × interquartile range). Parent–offspring interaction When considering all observation scans, we found that the time larvae spent begging as well as species, but not the interaction between the two, significantly affected parental provisioning (Table 3). For the subset of scans when at least one parent was close by, only larval begging had an effect on parental provisioning (Table 3). In all 3 species, there was a positive correlation between the overall time invested in begging and the overall time spent provisioning, both when all scans are considered (Pearson correlation: r = 0.88, n = 40, P < 0.001 for N. orbicollis; r = 0.86, n = 40, P < 0.001 for N. pustulatus; r = 0.96, n = 30, P < 0.001 for N. vespilloides, Figure 4), and when only those scans in which parents were in close proximity to larvae were included (Pearson correlation: r = 0.73, n = 40, P < 0.001 for N. orbicollis; r = 0.78, n = 40, P < 0.001 for N. pustulatus; r = 0.92, n = 30, P < 0.001 for N. vespilloides). Table 3 Results of LMMs of the effect of species (N. orbicollis, N. pustulatus, N. vespilloides) and the time spent begging by larvae and the interaction of factors on parental provisioning to larvae for scans when parents were in close proximity and for the whole observation period   Feeding parent/s present  Feeding all observation scans  Factor  X2  P  X2  P  Species  4.75  0.092  10.23  0.006  Larval begging  176.37  <0.001  521.93  <0.001  Species × larval begging  1.20  0.548  4.62  0.099    Feeding parent/s present  Feeding all observation scans  Factor  X2  P  X2  P  Species  4.75  0.092  10.23  0.006  Larval begging  176.37  <0.001  521.93  <0.001  Species × larval begging  1.20  0.548  4.62  0.099  Significant P values are typed in bold. View Large Figure 4 View largeDownload slide Correlation between the time spent begging (%) and the time spent provisioning (%) for scans when parents were in close proximity. (A) N. orbicollis. (B) N. pustulatus. (C) N. vespilloides. The shaded regions show the 95% confidence intervals. Figure 4 View largeDownload slide Correlation between the time spent begging (%) and the time spent provisioning (%) for scans when parents were in close proximity. (A) N. orbicollis. (B) N. pustulatus. (C) N. vespilloides. The shaded regions show the 95% confidence intervals. The average time parents spent in close proximity to their larvae significantly differed between the species (GLM with quasi-binomial errors: F1,52 = 5.15, P = 0.01, Figure 5). Parents of N. vespilloides spent more time near their larvae than parents of N. pustulatus (Tukey’s post-hoc test: P = 0.005). However, post-hoc comparisons showed that there was no difference in the time spent in close proximity to larvae between N. orbicollis and N. vespilloides (Tukey’s post-hoc test: P = 0.17), and N. orbicollis and N. pustulatus parents, respectively (Tukey’s post-hoc test: P = 0.28). Figure 5 View largeDownload slide The time parents spent in close proximity to their larvae (%). Boxplots show median, interquartile range, minimum/maximum range. The dots are values that fall outside the interquartile range (>1.5 × interquartile range). Figure 5 View largeDownload slide The time parents spent in close proximity to their larvae (%). Boxplots show median, interquartile range, minimum/maximum range. The dots are values that fall outside the interquartile range (>1.5 × interquartile range). Larval mass and time to dispersal Larval mass at hatching (0 h) differed significantly between the species. Larvae of N. orbicollis and N. vespilloides were similar in weight, and both were significantly heavier than larvae of N. pustulatus (GLM with Gaussian errors: F2,52 = 177.95, P < 0.001, Figure 6A). At 48 h, larvae of N. orbicollis and N. vespilloides were heavier than larvae of N. pustulatus, and larvae of N. vespilloides, in turn, were heavier than N. orbicollis larvae (GLM with Gaussian errors: F2,52 = 158.21, P < 0.001, Figure 6B). Finally, species also had an effect on larval mass at dispersal, with N. orbicollis and N. pustulatus larvae being significantly heavier than larvae of N. vespilloides (GLM with Gaussian errors: F2,52 = 59.79, P < 0.001, Figure 6C). Furthermore, we note that not all of the 15 larvae added survived to dispersal in each brood, and that survival at dispersal significantly differed between species (GLM with quasi-binomial errors: F2,52 = 4.49, P = 0.02). On average, larval survival in N. vespilloides (mean 9.8 ± SE 0.63) was higher than in N. orbicollis (mean 7.82 ± SE 0.44), but not significantly higher than in N. pustulatus (mean 8.45 ± SE 0.68). In addition, we found that the time to larval dispersal significantly differed between species (GLM with Gaussian errors: F2,52 = 72.22, P < 0.001). Larval N. orbicollis (mean 5.15 ± SE 0.14 days) as well as larval N. pustulatus (mean 5.5 ± SE 0.11 days) required fewer days until they dispersed from the carcass than larval N. vespilloides (mean 7.13 ± SE 0.09 days). Figure 6 View largeDownload slide Average larval mass (mg) of N. orbicollis, N. pustulatus and N. vespilloides at different points of time. (A) Initial larval mass at hatching (0 h). (B) Larval mass after 48 h on the carcass. (C) Final larval mass at dispersal. Boxplots show median, interquartile range, minimum/maximum range. The dots are values that fall outside the interquartile range (>1.5 × interquartile range). Figure 6 View largeDownload slide Average larval mass (mg) of N. orbicollis, N. pustulatus and N. vespilloides at different points of time. (A) Initial larval mass at hatching (0 h). (B) Larval mass after 48 h on the carcass. (C) Final larval mass at dispersal. Boxplots show median, interquartile range, minimum/maximum range. The dots are values that fall outside the interquartile range (>1.5 × interquartile range). DISCUSSION The time spent begging by larvae and the time spent provisioning by parents differed greatly between the 3 Nicrophorus species, and this aligned closely with the nutritional dependence of offspring on their parents. Larvae of N. pustulatus spent less time begging than larvae of N. orbicollis or larvae of N. vespilloides. In line with this, parents of N. pustulatus spent significantly less time provisioning than parents of N. orbicollis and N. vespilloides. In all 3 species, females provided significantly more food to larvae than their male partners. Below, we outline the potential selective factors leading to this diversification of larval begging and parental provisioning in relation to the distinct variation in offspring dependence among the 3 species. We predicted that the dependent offspring of N. orbicollis would invest the most in the time spent begging as the most food is needed to meet their nutritional requirements. Over the whole observation period, we found no difference between larval N. orbicollis and larval N. vespilloides in the time spent begging. However, in the presence of parents, larval N. orbicollis spent significantly more time begging than larval N. pustulatus, and also begged more than N. vespilloides. From a previous study, we know that larval N. orbicollis are highly dependent on parental care, whereas larvae of N. pustulatus appear to be nutritionally independent, and larval N. vespilloides show an intermediate dependence on parental care (Capodeanu-Nägler et al. 2016). Thus, our results strongly suggest that the intensity of larval begging in the 3 Nicrophorus species actually reflects the nutritional dependence of offspring. Consequently, instead of an arbitrary divergence in the intensity of begging behavior, we suggest that begging evolves according to intrinsic differences in the amount of food required to reach nutritional independence, and hence reflects both short-term and long-term needs (Price et al. 1996). There was a positive correlation between the time spent begging at 24 h and the time spent begging at 48 h in N. vespilloides, attesting to consistent differences among broods in begging rate. We did not, however, find this correlation in the other 2 species. We also found that larvae spent more time begging at 24 h than at 48 h in N. vespilloides. This is consistent with previous studies, which found that begging peaks at 24 h and decreases as the efficiency of larval self-feeding increases (Smiseth et al. 2003; Smiseth et al. 2007). It appears that there is not only a divergence in offspring begging rate between species, but also in the overall time period they spent begging. In contrast to N. vespilloides, larval N. orbicollis did not significantly reduce their begging behavior within the first 48 h, indicating that N. orbicollis larvae beg longer and are characterized by a longer period of dependency on parental food provisioning than N. vespilloides larvae. As theory predicts that the optimal timing for the transition from nutritional dependency to independence should differ between parents and offspring (Trivers 1974), it would be fruitful in future studies to determine when offspring terminate begging behavior across species and how parental removal before the end of the begging period affects offspring fitness. Previous work on N. orbicollis has revealed that parents spend more time provisioning offspring with increasing brood size, which indicates that parents respond to the amount of begging in the brood (Rauter and Moore 1999). However, a direct link between the time spent begging and investment in parental provisioning was shown only in later studies of N. vespilloides (Smiseth and Moore 2002; Lock et al. 2004). Likewise, our results show that the amount of begging positively correlates with the amount of provisioning within each of the 3 species. Interestingly, the slope of this relationship did not differ between the species, which means that in all 3 species an equivalent change in the amount of begging resulted in a similar change in parental response. Hence, the relation between solicitation behavior and parental provisioning has evolved in the same direction in all 3 species, or, alternatively, represents an ancestral state that has not diverged. However, besides these similarities, our study revealed that the species diverged in the overall magnitude of the begging stimulus that is required to trigger a response in parents. Despite caring for larvae that begged at a higher intensity than larvae of N. vespilloides, parents of N. orbicollis did not invest more time provisioning than parents of N. vespilloides. In other words, N. orbicollis larvae had to beg more to achieve similar provisioning rates as N. vespilloides offspring. In a cross-fostering experiment with N. orbicollis and N. vespilloides, Benowitz et al. (2015) also found no evidence that larval mass in the recipient species was dependent on the caregiving species. In a follow-up study, Benowitz et al. (2016) compared the parental behavior of N. orbicollis and N. vespilloides and found subtle variation in parenting between the 2 species. N. vespilloides provided less care overall, but parents were more likely to continue feeding once they had initiated it. Conversely, N. orbicollis parents were more likely to shift their behavior between feeding and other tasks (Benowitz et al. 2016). The authors suggested that this variation might reflect differences in larval behavior, with N. orbicollis larvae begging more intensively, thereby manipulating their parents into increased feeding. We were able to show that N. orbicollis larvae do indeed spend more time begging compared with the other 2 species. However, we did not find that parents of N. orbicollis spend more time provisioning than parents of N. vespilloides. At least 3 explanations could account for the discrepancy between larval begging and parental provisioning in N. orbicollis. First, parents of N. orbicollis may become increasingly resistant to larval begging and refrain from providing more food than necessary to ensure larval survival. Second, parents may be provisioning at their maximum capacity, making it unfeasible to further adjust the amount of feeding. Third, parents of N. orbicollis may transfer more food per provisioning event than parents of N. vespilloides. Our experimental design did not allow measurement of the nutritional value or the amount of food transferred, nor the time each single larva was provisioned during any one provisioning event. By counting the number of mouth-to-mouth contacts, we could only measure the frequency of provisioning. Steiger (2013) found that larger mothers are more efficient than smaller mothers at feeding offspring. In this regard, we note that N. orbicollis is the largest of the 3 species and can thus ingest and process more food per unit time than the 2 smaller species, allowing, perhaps, for more efficient food transfer. Consequently, it is possible that the amount of food transferred corresponds to begging intensity and the overall nutritional dependency of offspring across species. In species with biparental care, such as birds and mammals, females usually invest more in care than males (Kokko and Jennions 2008; Royle et al. 2016; Stockley and Hobson 2016). In burying beetles, males and females show the same repertoire of care behaviors and can be equally competent parents when providing care alone (Eggert and Müller 1997; Walling et al. 2008; Head et al. 2012). During biparental care, females usually specialize in performing direct care, such as feeding the offspring, whereas males mainly provide indirect care, such as maintaining and defending the carcass (Smiseth et al. 2005; Trumbo 2006; Walling et al. 2008). In our study, females of the 3 species provided significantly more food to larvae than their male counterparts. This implies that, apart from the principal differences in feeding behavior between the species, there were similar sex differences in provisioning within each species. This conforms to other studies on burying beetles, which found that when paired with a female, males generally show greater plasticity in parenting, but contribute less to care (Fetherston et al. 1990, 1994; Rauter and Moore 1999, 2004; Smiseth and Moore 2004b; Royle et al. 2014). Further, in N. vespilloides, maternal provisioning and offspring begging behavior are highly coordinated (Lock et al. 2004), whereas paternal provisioning and offspring begging behavior are not (Head et al. 2012). Interestingly, we found a divergence in the extent to which females and males contributed to provisioning between the species. Females of N. orbicollis spent more time provisioning than females of the other 2 species. However, male N. orbicollis were not as diligent as their female partner and contributed less to provisioning than N. vespilloides males. We can only speculate about the cause of this variation, but this uneven distribution may reflect differences in the strength of sexual conflict over parental investment in provisioning. To understand the striking variation in begging, provisioning and offspring dependency between species, we must also consider the different life-history strategies of burying beetles. For example, in a partial cross-fostering experiment, young of pied and collared flycatchers (Ficedula hypoleuca and Ficedula albicollis) have been shown to differ in their begging intensity (Qvarnström et al. 2007). The authors assumed that the difference in begging seems to honestly indicate intrinsic differences in the offspring that are likely linked to a differentiation in life-history traits. In the 3 species we examined, N. pustulatus is known to produce the largest number of offspring (Trumbo 1992; Capodeanu-Nägler et al. 2016). Thus, it may be necessary for offspring to maintain their independence as parents cannot attend to each larva as well as can parents of smaller broods (Trumbo 1992). Also, models predict that parental food provisioning only evolves if it is efficient relative to offspring self-feeding (Gardner and Smiseth 2011). In N. pustulatus, however, the large number of offspring (mean clutch size: 68 ± 19; see also Capodeanu-Nägler et al. 2016) hinders the efficient feeding of each larva in the brood, selecting against increased offspring dependency. In line with this, N. pustulatus parents provisioned significantly less than parents of the other 2 species. One other factor that could account for interspecific variation in begging, related to the nutritional dependence of offspring, is adult body size, as this is likely to influence growth rate and therefore offspring need. In burying beetles, larval weight at dispersal generally determines adult body size (Trumbo 1990) and we might expect that larger species are characterized by higher larval growth rate, which can only be accomplished by higher provisioning and begging efforts. Indeed, our results show that the 2 larger species, N. pustulatus and N. orbicollis, required less time for attaining their final body mass at dispersal than N. vespilloides, the smallest of the 3 species. However, this faster growth rate is not necessarily associated with a higher provisioning and begging rate, as begging intensity and levels of food provisioning were considerably lower in N. pustulatus than in N. vespilloides. Thus, when considering N. pustulatus, it seems rather unlikely that body size is the main determinant of how interactions between offspring and parents have evolved. Interestingly, although N. vespilloides larvae had overall the slowest growth rate, during the first 48 h, in which offspring begging and parental provisioning is most intense (Smiseth et al. 2003; Smiseth et al. 2007), they grew much faster than N. pustulatus larvae. Thus, while self-feeding in N. pustulatus appears to be sufficient to sustain the body functions of the hatchlings, parental provisioning in N. vespilloides seems to accelerate larval growth. Burying beetles represent an ideal model organism to explore the integration of offspring begging and parental provisioning once parental care has evolved because, within this genus, closely related species vary substantially in their reliance on parental food provisioning. Future studies might profitably employ cross-fostering among the 3 species to evaluate whether there is a positive correlation between offspring behavior of the recipient species and parental provisioning of the caregiving species. In combination with a consideration of various life-history strategies in this genus, this would help us to understand the emergence of the substantial differences in offspring dependence that have arisen within the genus. We recognize that the conclusions of our study are based on evidence derived from only 3 species, and are thus essentially qualitative with respect to between-species correlations. In a broader context, more comparative studies concerning offspring begging behavior and parental provisioning that also control for phylogeny are needed to further unravel the evolutionary trajectories and diversification of parental care. SUPPLEMENTARY MATERIAL Supplementary data are available at Behavioral Ecology online. FUNDING This work was supported by a grant from the German Research Foundation (DFG) to S.S. (grant number STE 1874/6-1) and a grant from the National Science Foundation (grant number IOS-1118160) to S.K.S. 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Species divergence in offspring begging and parental provisioning is linked to nutritional dependency

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Abstract

Abstract In animal species in which parents provide food to their dependent young, offspring often display conspicuous begging signals. These solicitation behaviors are important components of parent–offspring communication, but it is currently unclear how they and the parental response covary with offspring dependency on parental food provisioning across species. Burying beetles (Nicrophorus) are well known for providing elaborate biparental care, including provisioning of begging larvae. By using a multispecies approach, we show that larval begging intensity, as well as the time parents spend provisioning, differ greatly between individuals of the 3 species: N. orbicollis, N. pustulatus, and N. vespilloides. Our results demonstrate that the most dependent offspring of N. orbicollis invest the most time in begging, whereas the most independent offspring of N. pustulatus invest the least amount of time in begging. Thus, we suggest that begging intensity differs due to intrinsic differences in nutritional need between the species rather than because of an arbitrary divergence in begging behavior. We further show that in all 3 species, females spend significantly more time provisioning than males, although there is considerable divergence between species in the extent to which females and males contribute to the provisioning of larvae. We discuss the potential selective factors leading to this diversification of offspring begging and parental provisioning in relation to the distinct variation in offspring dependence between the 3 species. INTRODUCTION Communication between parents and offspring plays an essential role in animal species in which parents provide care to increase their offspring’s fitness (Clutton-Brock 1991). One important component of parent–offspring communication involves elaborate acoustic, visual, chemical, or tactile begging signals of offspring to solicit resources from caring parents (Kilner and Johnstone 1997). Such begging displays are supposed to reflect short-term need (i.e., hunger) of offspring that parents use to adjust their food allocation (e.g., Mock et al. 2011). Evidence for intense interactions between parental provisioning and offspring begging mainly comes from studies on birds or mammals (Kilner and Johnstone 1997). In several bird species, for example, food-deprived chicks have been shown to beg more intensively than well-fed chicks to advertise their hunger level to caring parents (e.g., Mondloch 1995; Price and Ydenberg 1995). However, the intensity of begging may also depend on the total amount of food required prior to independence, which is often referred to as the long-term need (Price et al. 1996). Given the same feeding rate and amount, offspring with an overall higher long-term need are expected to beg more intensively. In fact, evidence in support of this proposition comes from a study on yellow headed blackbirds (Price et al. 1996). As begging should influence offspring growth and survival, and the magnitude of this effect in turn depends on how dependent the offspring are on their parents’ food (i.e., the overall fitness benefit of receiving parental food), the degree of offspring dependency must be considered to understand the evolutionary interplay between begging signals and parental response to these signals. We would, for example, predict offspring to vary in their intensity of begging according to how dependent they are on parental provisioning, both within and between species. There are, however, few studies that have explored the divergence in begging behavior between different species. In a partial cross-fostering experiment, Qvarnström et al. (2007) found that young of pied and collared flycatchers (Ficedula hypoleuca and Ficedula albicollis) showed a strong difference in their begging intensity, suggesting that the observed difference in begging intensity reflects a genetic difference in offspring need to which the parents of both species respond. Although this latter study certainly demonstrates between-species variation in begging intensity, it does not allow any conclusions about how begging behavior covaries with how dependent the offspring are on parental provisioning. From a behavioral and evolutionary viewpoint, it is important to consider offspring begging together with the parental response to begging, that is, the amount of food provided. As parental provisioning and offspring begging reciprocally influence each other, both traits are expected to coevolve and may become genetically correlated, ultimately leading to coadaptation of parental and offspring traits (Wolf and Brodie 1998; Kölliker et al. 2005; Meunier and Kölliker 2012). As the coevolution of supply (parental provisioning) and demand (offspring begging) can generate a positive or a negative correlation between parent and offspring traits, depending on whether parents or offspring are in control of food allocation (Kölliker et al. 2005; Smiseth et al. 2008; Hinde et al. 2010), the outcome of this coevolution might differ. The coevolutionary trajectory of provisioning and begging intensity might diverge between species according to genetic differences in need or arbitrarily due to differences in the escalation of parent–offspring conflict. Thus, to investigate the early evolution of provisioning and begging, a multispecies approach, involving different species that vary in the ability of offspring to self-feed and their concomitant reliance on parental provisioning, could be highly informative. Furthermore, greater offspring demand might select for higher provisioning rates in both parents, or, alternatively, only one of the sexes might be targeted. In general, it is important to consider that the evolutionary interests of male and female parents over parental investment often do not coincide (Trivers 1972). Consequently, sex differences in food provisioning may arise and one sex might be more responsive to offspring begging than the other. Across diverse animal taxa, females are known to provide more care than males, and there is evidence from birds, mammals and insects that males and females differ in their response to offspring begging (Kölliker et al. 1998; Kilner 2002; Quillfeldt et al. 2004; Smiseth and Moore 2004a; English et al. 2008). Nevertheless, the degree of sex differences in offspring provisioning might vary across closely related species, that is, there might be species in which both parents are nearly equally responsive to offspring begging, whereas in others, one of the sexes might do the majority of the work. Differences between males and females in the decision rules regarding parental provisioning could greatly influence the fitness of dependent offspring, and thus it could be fruitful to examine whether such sex differences in parental provisioning vary across species. Burying beetles of the genus Nicrophorus are well known for exploiting small vertebrate carcasses and providing extensive biparental care to their offspring including regurgitation of carrion (Pukowski 1933; Eggert and Müller 1997; Eggert et al. 1998; Scott 1998). Larvae can feed independently, but also beg for predigested food by raising their head toward the parent while waving their legs or touching the parent with their legs (Rauter and Moore 1999; Smiseth et al. 2003). Previous studies on burying beetles have found that begging reflects an offspring’s hunger level (Smiseth and Moore 2004b), and that larvae adjust the time spent begging according to brood size and behavior of competing siblings and caring parents (Rauter and Moore 1999; Smiseth and Moore 2002), as well as their proficiency at self-feeding (Smiseth et al. 2003). Larvae have also been shown to beg only when a parent is nearby (Rauter and Moore 1999; Smiseth and Moore 2002). In turn, parents respond to begging by adjusting the time spent allocating resources to offspring (Smiseth and Moore 2002, 2008). We recently showed that offspring of 3 species, N. orbicollis, N. pustulatus, and N. vespilloides, show striking variation in their reliance on parental care (Capodeanu-Nägler et al. 2016). In that study, we manipulated the occurrence of prehatching (no care or care) and/or posthatching care (no care or care) in each of the 3 species and found a differential reliance on posthatching care, which consists mainly of food provisioning, but not on the prehatching component of parental care. In the majority of cases, none of the larval N. orbicollis survived in the absence of parental feeding, indicating obligate parental care in this species. In contrast, in N. pustulatus, larval survival and growth was not reduced in the absence of parents. The reliance of N. vespilloides larvae on posthatching care appears to be intermediate, as offspring survival and growth in the absence of posthatching care was better than in N. orbicollis, but worse than in N. pustulatus. Consequently, these results indicate that there are contrasting nutritional requirements, and that the fitness benefits of food provisioning differ between the offspring of the 3 species. In the present multispecies study, we tested the hypothesis that offspring of the 3 Nicrophorus species vary in their amount of begging and that parents, in turn, have adapted to respond to this variation by modulating the amount of food provided. If begging intensity of larvae is related to the degree of offspring dependence and the offspring’s need for nutritional resources, we further predicted that larvae of N. orbicollis, which show the strongest reliance on parental care, would also display the strongest begging behavior to solicit more food from their parents. In contrast, N. pustulatus offspring that appear to be nutritionally independent of their parents are predicted to beg less and to be fed the least by their parents. We predicted that N. vespilloides, in which larvae are only partially dependent on parental provisioning, would show an intermediate amount of begging and provisioning behavior. We additionally tested for sex differences in the time spent provisioning the larvae, as previous studies have shown that females spend more time feeding the larvae than males (Fetherston et al. 1990, 1994; Rauter and Moore 1999, 2004; Smiseth and Moore 2004b). MATERIALS AND METHODS Origin and maintenance of experimental animals Experimental N. vespilloides were descendants of beetles collected from carrion-baited pitfall traps in a forest near Ulm, Germany (48°25′03′′N, 9°57′45′′E). Cultures of N. pustulatus and N. orbicollis were established at Ulm University from outbred colonies maintained at the Institute of Zoology, University of Freiburg, Germany. We maintained outbred colonies of both species by introducing beetles captured in baited pitfall traps established in a forested area near Lexington, IL (40°39′57′′N, 88°53′49′′W). All beetles were maintained in temperature-controlled chambers at 20 °C on a 16:8 h light:dark cycle. Before the experiments, groups of up to 5 adults of the same sex and family of each species were kept in small plastic containers (10 × 10 cm and 6 cm high) filled with moist peat. Beetles were fed freshly decapitated mealworms ad libitum twice a week. At the time of experiments, beetles were virgin and between 30 and 40 days of age. Experimental design For our study, nonsibling pairs of beetles were randomly paired and reproduction was induced by providing them with a 20 g (± 3 g) thawed mouse carcass (Frostfutter.de—B.A.F Group GmbH, Germany). In the case of the nocturnal species, N. pustulatus and N. orbicollis, mice were provided during the dark portion of the photoperiod. After the egg-laying period, but before larvae hatched (see Capodeanu-Nägler et al. 2016), parents and the carcass were transferred to new plastic containers filled with soil. The eggs were left to hatch in the old container, which we checked every 8 h for the presence of newly hatched larvae. We weighed the larvae when they hatched (0 h), before providing each pair of beetles with a brood of 15 newly hatched larvae of mixed parentage to control for variation between families and individual differences in behavior (Rauter and Moore 1999). As brood size is known to affect larval begging (Smiseth and Moore 2002; Smiseth et al. 2007) as well as parental provisioning (Rauter and Moore 1999; but see Smiseth and Moore 2002), we opted for a standardized brood size of 15 larvae. The larvae were placed directly onto the carcass, which we had sliced open earlier to facilitate their access to the carrion. As females exhibit temporally-based kin discrimination in which they kill any larvae arriving on the carcass before their own eggs would have hatched, but accept larvae that arrive after their own eggs have begun to hatch (Müller and Eggert 1990), we provided pairs with larvae only after their own larvae had begun hatching. We established broods until attaining a minimum sample size of 15 for each species (n = 20 for N. orbicollis, n = 20 for N. pustulatus, n = 15 for N. vespilloides). We conducted behavioral observations on larval begging and parental food provisioning at 24 and 48 h, respectively, when larvae have reached the second instar and larval begging is known to peak (Smiseth and Moore 2002; Smiseth et al. 2003). We used instantaneous scan sampling every 1 min for 30 min (Martin and Bateson 1986) to record larval and parental behavior (Rauter and Moore 1999). To facilitate discrimination between the sexes, we marked males with a dot of white correction fluid on one elytron and a dot on the pronotum (Rauter and Moore 2002). At each scan, we recorded the following traits and behaviors: 1) The number of larvae that were begging. A larva was considered to be begging when it raised its head towards the parent while waving its legs, or touched the parent with its legs (Rauter and Moore 1999; Smiseth and Moore 2002). 2) The number of mouth-to-mouth contacts between a parent and at least one larva, indicating parental provisioning. 3) The sex of the parent providing food to the larvae. 4) The proximity of parents to the larvae, defined as the distance less than the width of the parent’s pronotum from the larvae, as larvae begin begging only when a parent is close by (Rauter and Moore 1999; Smiseth and Moore 2002). Before beginning observations, we covered each box containing parents, larvae and the carcass with a thin glass panel (12 × 12 cm), allowing individuals to acclimatize for 15 min. We weighed the larvae of each brood at 2 additional time points, at the end of the 48-h observation period, and upon their dispersal from the carcass. Statistics All data were analyzed and plotted using R version 3.1.2 (R Core Team 2014). For larval begging behavior, we calculated the average percentage of time spent begging by larvae in each brood, bi, as bi = ∑b/L × 100/30, where b is the total number of larval begging events during the 30 scans of an observation session, and L is the brood size (Smiseth and Moore 2002, 2004b), which in our experiments always corresponded to a brood size of 15 larvae. As larvae beg only when parents are close by, we also calculated the average percentage of larval begging time in the presence of parents as a second parameter (Smiseth and Moore 2004b). For this metric, we replaced the total number of 30 observation scans in the formula with the number of scans when at least one of the parents was in close proximity to the larvae. For calculating parental food provisioning, we used the same formula as for larval begging behavior, replacing the total number of begging events bi with the total number of mouth-to-mouth-contacts for all 30 scans, as well as for all scans when at least one of the parents was in close proximity. By using the lmer function from the lme4 package, we then performed linear mixed-effect models (LMMs) in which we included brood ID as a random factor to control for repeated measurements in our design. We used species, the time of observation and species × time of observation as fixed factors, and the average percentage of larval begging time during all observations (30 scans), the average percentage of larval begging time when parents were in close proximity, the average percentage of parental food provisioning during all observations, and the average percentage of parental food provisioning when parents were in close proximity as dependent variables. To localize species-specific differences, we then continued with simpler generalized linear models (GLMs) followed by post-hoc Tukey comparisons in which species was included as a fixed factor with the same dependent variables as described above. Within species, we also performed GLMs in which we included the sex of the provisioning parent, time of observation, and the interaction between sex and time as fixed factors, and each of the parameters measuring parental food provisioning as dependent variables. In addition, we performed GLMs within species with the time of observation as a fixed factor, and both parameters measuring begging behavior as dependent variables. Further, we calculated the proportion of time that parents stayed in close proximity to the larvae relative to the total number of all observation scans by creating a 2-column response vector consisting of the number of positives (i.e., parents in close proximity) and the number of negatives (parents not in close proximity) joined together by the function cbind. We then applied GLMs with a quasi-binomial distribution. The same statistical approach was used to compare larval survival (i.e., larvae survived vs. larvae not survived) at dispersal. We compared the mean larval mass per brood of the species at different points in development (0 h, 48 h, and upon dispersal of the larvae), and the time until larval dispersal by using GLMs with a Gaussian distribution. RESULTS Larval begging behavior We found significant effects of species and the time of observation as well as an interaction of both effects on larval begging behavior (Table 1). When parents were in close proximity to larvae, begging behavior differed significantly between larvae of all 3 species (Table 1; Figure 1). Larvae of N. orbicollis spent more time begging than larvae of N. pustulatus (Tukey’s post-hoc test: P < 0.001) and N. vespilloides (Tukey’s post-hoc test: P = 0.01). In addition, N. vespilloides larvae spent more time begging than N. pustulatus larvae (Tukey’s post hoc test: P < 0.001). With respect to all scans during an observation session irrespective of parental proximity, begging behavior still significantly differed between larvae of the 3 species (Table 1; Supplementary Figure S1). However, post-hoc comparisons showed that there was no longer a significant difference between the time invested in begging by N. orbicollis and N. vespilloides larvae (Tukey’s post-hoc test: P = 0.19). Table 1 Results of LMMs of the effect of species (N. orbicollis, N. pustulatus, N. vespilloides), time of observation (24 h or 48 h), and the interaction of species and time of observation on larval begging for scans when parents were in close proximity and for the whole observation period   Begging parent/s present  Begging all observation scans  Factor  X2  P  X2  P  Species  88.01  <0.001  58.99  <0.001  Time of observation  12.26  <0.001  7.70  0.006  Species × time of observation  8.52  0.014  12.96  0.002    Begging parent/s present  Begging all observation scans  Factor  X2  P  X2  P  Species  88.01  <0.001  58.99  <0.001  Time of observation  12.26  <0.001  7.70  0.006  Species × time of observation  8.52  0.014  12.96  0.002  Significant P values are typed in bold. View Large Figure 1 View largeDownload slide The time spent begging by each larva (%) when parents were in close proximity at 24 h and 48 h. Boxplots show median, interquartile range, minimum/maximum range. The dots are values that fall outside the interquartile range (>1.5 × interquartile range). Figure 1 View largeDownload slide The time spent begging by each larva (%) when parents were in close proximity at 24 h and 48 h. Boxplots show median, interquartile range, minimum/maximum range. The dots are values that fall outside the interquartile range (>1.5 × interquartile range). Time of observation (24 h or 48 h) had an effect on begging, but this effect differed between the species (Table 1). For both begging parameters, we found that N. vespilloides and N. orbicollis larvae reduce begging from 24 h to 48 h, whereas larval N. pustulatus tend to increase begging. To better understand how time affects begging, we analyzed the species separately. In N. orbicollis and N. pustulatus, the time of observation had no effect on the average time larvae spent begging, regardless of whether all scans in an observation session were included (GLM with Gaussian errors: F1,38 = 0.29, P = 0.59 for N. orbicollis; F1,38 = 0.17, P = 0.68 for N. pustulatus) or only those scans when at least one parent was in close proximity (GLM with Gaussian errors: F1,38 = 3.27, P = 0.08 for N. orbicollis; F1,38 = 0.02, P = 0.89 for N. pustulatus, Supplementary Figure S2). Also, in both species, there was no significant correlation between the time invested in begging at 24 h and the time invested in begging at 48 h, both when all observation scans were considered (Pearson correlation: r = 0.36, n = 40, P = 0.12 for N. orbicollis; r = 0.09, n = 40, P = 0.71 for N. pustulatus) and when only those scans when parents were close by were included (Pearson correlation: r = 0.25, n = 40, P = 0.28 for N. orbicollis; r = 0.09, n = 40, P = 0.70 for N. pustulatus). In N. vespilloides, we found that the same brood that invested a lot of time in begging at 24 h also invested more time at 48 h, whereas broods that invested less time in begging at 24 h also invested less time at 48 h. This was true for all observation scans (Pearson correlation: r = 0.58, n = 30, P = 0.02), as well as for the scans in which parents were in close proximity (Pearson correlation: r = 0.53, n = 30, P = 0.04, Supplementary Figure S2). For both begging parameters, the time of observation had a negative effect on larval begging behavior in N. vespilloides (GLM with Gaussian errors: F1,28 = 14.26, P < 0.001 for all observation scans; F1,28 = 12.28, P = 0.002 for scans with parents present only). On average, larvae reduced begging, that is, they begged at lower intensities at 48 h than after 24 h of development. Parental food provisioning We found that species but not the time of observation significantly affected parental food provisioning (Table 2). Furthermore, the interaction between species and time of observation had a significant effect on parental provisioning (Table 2). Food provisioning from parents to larvae differed significantly between the 3 species, regardless of whether we included all scans of an observation session (Table 2; Supplementary Figure S3) or only those scans in which parents were in close proximity to larvae (Table 2; Figure 2). Parents of N. pustulatus invested the least amount of time feeding their larvae. There was no difference in the time spent provisioning between parents of N. orbicollis and parents of N. vespilloides (Tukey’s post-hoc test: P = 0.96 for all observation scans; P = 0.55 for scans with parents present only). Table 2 Results of LMMs of the effect of species (N. orbicollis, N. pustulatus, N. vespilloides) and the time of observation (24 h or 48 h) and the interaction of factors on parental feeding to larvae for scans when parents were in close proximity and for the whole observation period   Feeding parent/s present  Feeding all observation scans  Factor  X2  P  X2  P  Species  47.90  <0.001  43.55  <0.001  Time of observation  1.91  0.167  1.53  0.216  Species × time of observation  10.03  0.007  21.69  <0.001    Feeding parent/s present  Feeding all observation scans  Factor  X2  P  X2  P  Species  47.90  <0.001  43.55  <0.001  Time of observation  1.91  0.167  1.53  0.216  Species × time of observation  10.03  0.007  21.69  <0.001  Significant P values are typed in bold. View Large Figure 2 View largeDownload slide The time parents spent provisioning larvae (%) for scans when parents were in close proximity at 24 h and 48 h. Boxplots show median, interquartile range, minimum/maximum range. The dots are values that fall outside the interquartile range (>1.5 × interquartile range). Figure 2 View largeDownload slide The time parents spent provisioning larvae (%) for scans when parents were in close proximity at 24 h and 48 h. Boxplots show median, interquartile range, minimum/maximum range. The dots are values that fall outside the interquartile range (>1.5 × interquartile range). Time of observation (24 h or 48 h) had an effect on parental provisioning, but this effect differed between the species (Table 2). Parental provisioning did not change with offspring age in N. orbicollis, whereas it clearly decreased in N. vespilloides and tended to increase in N. pustulatus. To better understand how time affects parental provisioning, we analyzed the species separately. In N. orbicollis and N. pustulatus, the time of observation had no effect on the average time parents spent provisioning, regardless of whether we included all scans of an observation session (GLM with Gaussian errors: F1,58 = 0.20, P = 0.65 for N. orbicollis; F1,32 = 0.84, P = 0.37 for N. pustulatus), or the subset of scans when at least one parent was close by (GLM with Gaussian errors: F1,58 = 2.05, P = 0.16 for N. orbicollis; F1,32 = 0.37, P = 0.55 for N. pustulatus; Supplementary Figure S5). There was no significant correlation between the time invested in provisioning at 24 h and the time invested in provisioning at 48 h in either species, both when all observation scans were considered (Pearson correlation: r = 0.36, n = 40, P = 0.12 for N. orbicollis; r = 0.09, n = 40, P = 0.71 for N. pustulatus) and in the subset of scans when parents were close by (Pearson correlation: r = 0.25, n = 40, P = 0.28 for N. orbicollis; r = 0.09, n = 40, P = 0.70 for N. pustulatus). In N. vespilloides, parents spent significantly more time provisioning at 24 h than at 48 h, both when all observation scans are considered (GLM with Gaussian errors: F1,54 = 12.58, P < 0.001), and in the subset of scans when parents were in close proximity (GLM with Gaussian errors: F1,54 = 9.72, P = 0.003; Supplementary Figure S5). However, for both provisioning parameters, there was no correlation between the time a N. vespilloides parent invested in provisioning at 24 h and the time it invested in provisioning at 48 h (Pearson correlation: r = 0.50, n = 30, P = 0.06 for all observation scans; r = 0.37, n = 30, P = 0.18 for scans with parents present only). This is also true if we consider females (Pearson correlation: r = 0.29, n = 15, P = 0.30 for all observation scans; r = 0.42, n = 15, P = 0.12 for scans with parents present only) and males separately (Pearson correlation: r = −0.09, n = 15, P = 0.74 for all observation scans; r = −0.03, n = 15, P = 0.92 for scans with parents present only). The interaction between the sex of the provisioning parent and the time of observation was not statistically significant, regardless of whether we included all scans of an observation session (GLM with Gaussian errors: F1,58 = 0.04, P = 0.84 for N. orbicollis; F1,32 = 1.06, P = 0.31 for N. pustulatus; F1,54 = 1.57, P = 0.22 for N. vespilloides) or the subset of scans in which parents were in close proximity to larvae (GLM with Gaussian errors: F1,58 = 3.11, P = 0.08 for N. orbicollis; F1,32 = 0.51, P = 0.48 for N. pustulatus; F1,54 = 0.33, P = 0.57 for N. vespilloides). Within each of the 3 species, the female parent spent significantly more time provisioning larvae than the male parent. This was true when all scans in an observation session were included (GLM with Gaussian errors: F1,58 = 77.49, P < 0.001 for N. orbicollis; F1,32 = 23.52, P < 0.001 for N. pustulatus; F1,54 = 13.78, P = 0.001 for N. vespilloides, Supplementary Figure S4), and in the subset of scans when at least one of the parents was close by (GLM with Gaussian errors: F1,58 = 125.00, P < 0.001 for N. orbicollis; F1,32 = 21.52, P < 0.001 for N. pustulatus; F1,54 = 18.38, P < 0.001 for N. vespilloides, Figure 3). Interestingly, we found interspecific differences in the time spent provisioning when analyzing each sex independently (GLM with Gaussian errors: F2,75 = 6.65, P = 0.002 for males; F2,75 = 23.10, P < 0.001 for females). For scans in which parents were in close proximity, male N. vespilloides provided significantly more food than male N. orbicollis (Tukey’s post-hoc test: P = 0.03) and male N. pustulatus (Tukey’s post-hoc test: P = 0.001). In contrast, female N. orbicollis spent significantly more time provisioning than female N. pustulatus (Tukey’s post-hoc test: P < 0.001) and female N. vespilloides (Tukey’s post-hoc test: P < 0.001). We also found that female N. vespilloides spent more time feeding than female N. pustulatus when analyzing all observation scans (Tukey’s post-hoc test: P = 0.02). Figure 3 View largeDownload slide Sex differences in the time spent provisioning the larvae (%) for scans when parents were in close proximity. Boxplots show median, interquartile range, minimum/maximum range. The dots are values that fall outside the interquartile range (>1.5 × interquartile range). Figure 3 View largeDownload slide Sex differences in the time spent provisioning the larvae (%) for scans when parents were in close proximity. Boxplots show median, interquartile range, minimum/maximum range. The dots are values that fall outside the interquartile range (>1.5 × interquartile range). Parent–offspring interaction When considering all observation scans, we found that the time larvae spent begging as well as species, but not the interaction between the two, significantly affected parental provisioning (Table 3). For the subset of scans when at least one parent was close by, only larval begging had an effect on parental provisioning (Table 3). In all 3 species, there was a positive correlation between the overall time invested in begging and the overall time spent provisioning, both when all scans are considered (Pearson correlation: r = 0.88, n = 40, P < 0.001 for N. orbicollis; r = 0.86, n = 40, P < 0.001 for N. pustulatus; r = 0.96, n = 30, P < 0.001 for N. vespilloides, Figure 4), and when only those scans in which parents were in close proximity to larvae were included (Pearson correlation: r = 0.73, n = 40, P < 0.001 for N. orbicollis; r = 0.78, n = 40, P < 0.001 for N. pustulatus; r = 0.92, n = 30, P < 0.001 for N. vespilloides). Table 3 Results of LMMs of the effect of species (N. orbicollis, N. pustulatus, N. vespilloides) and the time spent begging by larvae and the interaction of factors on parental provisioning to larvae for scans when parents were in close proximity and for the whole observation period   Feeding parent/s present  Feeding all observation scans  Factor  X2  P  X2  P  Species  4.75  0.092  10.23  0.006  Larval begging  176.37  <0.001  521.93  <0.001  Species × larval begging  1.20  0.548  4.62  0.099    Feeding parent/s present  Feeding all observation scans  Factor  X2  P  X2  P  Species  4.75  0.092  10.23  0.006  Larval begging  176.37  <0.001  521.93  <0.001  Species × larval begging  1.20  0.548  4.62  0.099  Significant P values are typed in bold. View Large Figure 4 View largeDownload slide Correlation between the time spent begging (%) and the time spent provisioning (%) for scans when parents were in close proximity. (A) N. orbicollis. (B) N. pustulatus. (C) N. vespilloides. The shaded regions show the 95% confidence intervals. Figure 4 View largeDownload slide Correlation between the time spent begging (%) and the time spent provisioning (%) for scans when parents were in close proximity. (A) N. orbicollis. (B) N. pustulatus. (C) N. vespilloides. The shaded regions show the 95% confidence intervals. The average time parents spent in close proximity to their larvae significantly differed between the species (GLM with quasi-binomial errors: F1,52 = 5.15, P = 0.01, Figure 5). Parents of N. vespilloides spent more time near their larvae than parents of N. pustulatus (Tukey’s post-hoc test: P = 0.005). However, post-hoc comparisons showed that there was no difference in the time spent in close proximity to larvae between N. orbicollis and N. vespilloides (Tukey’s post-hoc test: P = 0.17), and N. orbicollis and N. pustulatus parents, respectively (Tukey’s post-hoc test: P = 0.28). Figure 5 View largeDownload slide The time parents spent in close proximity to their larvae (%). Boxplots show median, interquartile range, minimum/maximum range. The dots are values that fall outside the interquartile range (>1.5 × interquartile range). Figure 5 View largeDownload slide The time parents spent in close proximity to their larvae (%). Boxplots show median, interquartile range, minimum/maximum range. The dots are values that fall outside the interquartile range (>1.5 × interquartile range). Larval mass and time to dispersal Larval mass at hatching (0 h) differed significantly between the species. Larvae of N. orbicollis and N. vespilloides were similar in weight, and both were significantly heavier than larvae of N. pustulatus (GLM with Gaussian errors: F2,52 = 177.95, P < 0.001, Figure 6A). At 48 h, larvae of N. orbicollis and N. vespilloides were heavier than larvae of N. pustulatus, and larvae of N. vespilloides, in turn, were heavier than N. orbicollis larvae (GLM with Gaussian errors: F2,52 = 158.21, P < 0.001, Figure 6B). Finally, species also had an effect on larval mass at dispersal, with N. orbicollis and N. pustulatus larvae being significantly heavier than larvae of N. vespilloides (GLM with Gaussian errors: F2,52 = 59.79, P < 0.001, Figure 6C). Furthermore, we note that not all of the 15 larvae added survived to dispersal in each brood, and that survival at dispersal significantly differed between species (GLM with quasi-binomial errors: F2,52 = 4.49, P = 0.02). On average, larval survival in N. vespilloides (mean 9.8 ± SE 0.63) was higher than in N. orbicollis (mean 7.82 ± SE 0.44), but not significantly higher than in N. pustulatus (mean 8.45 ± SE 0.68). In addition, we found that the time to larval dispersal significantly differed between species (GLM with Gaussian errors: F2,52 = 72.22, P < 0.001). Larval N. orbicollis (mean 5.15 ± SE 0.14 days) as well as larval N. pustulatus (mean 5.5 ± SE 0.11 days) required fewer days until they dispersed from the carcass than larval N. vespilloides (mean 7.13 ± SE 0.09 days). Figure 6 View largeDownload slide Average larval mass (mg) of N. orbicollis, N. pustulatus and N. vespilloides at different points of time. (A) Initial larval mass at hatching (0 h). (B) Larval mass after 48 h on the carcass. (C) Final larval mass at dispersal. Boxplots show median, interquartile range, minimum/maximum range. The dots are values that fall outside the interquartile range (>1.5 × interquartile range). Figure 6 View largeDownload slide Average larval mass (mg) of N. orbicollis, N. pustulatus and N. vespilloides at different points of time. (A) Initial larval mass at hatching (0 h). (B) Larval mass after 48 h on the carcass. (C) Final larval mass at dispersal. Boxplots show median, interquartile range, minimum/maximum range. The dots are values that fall outside the interquartile range (>1.5 × interquartile range). DISCUSSION The time spent begging by larvae and the time spent provisioning by parents differed greatly between the 3 Nicrophorus species, and this aligned closely with the nutritional dependence of offspring on their parents. Larvae of N. pustulatus spent less time begging than larvae of N. orbicollis or larvae of N. vespilloides. In line with this, parents of N. pustulatus spent significantly less time provisioning than parents of N. orbicollis and N. vespilloides. In all 3 species, females provided significantly more food to larvae than their male partners. Below, we outline the potential selective factors leading to this diversification of larval begging and parental provisioning in relation to the distinct variation in offspring dependence among the 3 species. We predicted that the dependent offspring of N. orbicollis would invest the most in the time spent begging as the most food is needed to meet their nutritional requirements. Over the whole observation period, we found no difference between larval N. orbicollis and larval N. vespilloides in the time spent begging. However, in the presence of parents, larval N. orbicollis spent significantly more time begging than larval N. pustulatus, and also begged more than N. vespilloides. From a previous study, we know that larval N. orbicollis are highly dependent on parental care, whereas larvae of N. pustulatus appear to be nutritionally independent, and larval N. vespilloides show an intermediate dependence on parental care (Capodeanu-Nägler et al. 2016). Thus, our results strongly suggest that the intensity of larval begging in the 3 Nicrophorus species actually reflects the nutritional dependence of offspring. Consequently, instead of an arbitrary divergence in the intensity of begging behavior, we suggest that begging evolves according to intrinsic differences in the amount of food required to reach nutritional independence, and hence reflects both short-term and long-term needs (Price et al. 1996). There was a positive correlation between the time spent begging at 24 h and the time spent begging at 48 h in N. vespilloides, attesting to consistent differences among broods in begging rate. We did not, however, find this correlation in the other 2 species. We also found that larvae spent more time begging at 24 h than at 48 h in N. vespilloides. This is consistent with previous studies, which found that begging peaks at 24 h and decreases as the efficiency of larval self-feeding increases (Smiseth et al. 2003; Smiseth et al. 2007). It appears that there is not only a divergence in offspring begging rate between species, but also in the overall time period they spent begging. In contrast to N. vespilloides, larval N. orbicollis did not significantly reduce their begging behavior within the first 48 h, indicating that N. orbicollis larvae beg longer and are characterized by a longer period of dependency on parental food provisioning than N. vespilloides larvae. As theory predicts that the optimal timing for the transition from nutritional dependency to independence should differ between parents and offspring (Trivers 1974), it would be fruitful in future studies to determine when offspring terminate begging behavior across species and how parental removal before the end of the begging period affects offspring fitness. Previous work on N. orbicollis has revealed that parents spend more time provisioning offspring with increasing brood size, which indicates that parents respond to the amount of begging in the brood (Rauter and Moore 1999). However, a direct link between the time spent begging and investment in parental provisioning was shown only in later studies of N. vespilloides (Smiseth and Moore 2002; Lock et al. 2004). Likewise, our results show that the amount of begging positively correlates with the amount of provisioning within each of the 3 species. Interestingly, the slope of this relationship did not differ between the species, which means that in all 3 species an equivalent change in the amount of begging resulted in a similar change in parental response. Hence, the relation between solicitation behavior and parental provisioning has evolved in the same direction in all 3 species, or, alternatively, represents an ancestral state that has not diverged. However, besides these similarities, our study revealed that the species diverged in the overall magnitude of the begging stimulus that is required to trigger a response in parents. Despite caring for larvae that begged at a higher intensity than larvae of N. vespilloides, parents of N. orbicollis did not invest more time provisioning than parents of N. vespilloides. In other words, N. orbicollis larvae had to beg more to achieve similar provisioning rates as N. vespilloides offspring. In a cross-fostering experiment with N. orbicollis and N. vespilloides, Benowitz et al. (2015) also found no evidence that larval mass in the recipient species was dependent on the caregiving species. In a follow-up study, Benowitz et al. (2016) compared the parental behavior of N. orbicollis and N. vespilloides and found subtle variation in parenting between the 2 species. N. vespilloides provided less care overall, but parents were more likely to continue feeding once they had initiated it. Conversely, N. orbicollis parents were more likely to shift their behavior between feeding and other tasks (Benowitz et al. 2016). The authors suggested that this variation might reflect differences in larval behavior, with N. orbicollis larvae begging more intensively, thereby manipulating their parents into increased feeding. We were able to show that N. orbicollis larvae do indeed spend more time begging compared with the other 2 species. However, we did not find that parents of N. orbicollis spend more time provisioning than parents of N. vespilloides. At least 3 explanations could account for the discrepancy between larval begging and parental provisioning in N. orbicollis. First, parents of N. orbicollis may become increasingly resistant to larval begging and refrain from providing more food than necessary to ensure larval survival. Second, parents may be provisioning at their maximum capacity, making it unfeasible to further adjust the amount of feeding. Third, parents of N. orbicollis may transfer more food per provisioning event than parents of N. vespilloides. Our experimental design did not allow measurement of the nutritional value or the amount of food transferred, nor the time each single larva was provisioned during any one provisioning event. By counting the number of mouth-to-mouth contacts, we could only measure the frequency of provisioning. Steiger (2013) found that larger mothers are more efficient than smaller mothers at feeding offspring. In this regard, we note that N. orbicollis is the largest of the 3 species and can thus ingest and process more food per unit time than the 2 smaller species, allowing, perhaps, for more efficient food transfer. Consequently, it is possible that the amount of food transferred corresponds to begging intensity and the overall nutritional dependency of offspring across species. In species with biparental care, such as birds and mammals, females usually invest more in care than males (Kokko and Jennions 2008; Royle et al. 2016; Stockley and Hobson 2016). In burying beetles, males and females show the same repertoire of care behaviors and can be equally competent parents when providing care alone (Eggert and Müller 1997; Walling et al. 2008; Head et al. 2012). During biparental care, females usually specialize in performing direct care, such as feeding the offspring, whereas males mainly provide indirect care, such as maintaining and defending the carcass (Smiseth et al. 2005; Trumbo 2006; Walling et al. 2008). In our study, females of the 3 species provided significantly more food to larvae than their male counterparts. This implies that, apart from the principal differences in feeding behavior between the species, there were similar sex differences in provisioning within each species. This conforms to other studies on burying beetles, which found that when paired with a female, males generally show greater plasticity in parenting, but contribute less to care (Fetherston et al. 1990, 1994; Rauter and Moore 1999, 2004; Smiseth and Moore 2004b; Royle et al. 2014). Further, in N. vespilloides, maternal provisioning and offspring begging behavior are highly coordinated (Lock et al. 2004), whereas paternal provisioning and offspring begging behavior are not (Head et al. 2012). Interestingly, we found a divergence in the extent to which females and males contributed to provisioning between the species. Females of N. orbicollis spent more time provisioning than females of the other 2 species. However, male N. orbicollis were not as diligent as their female partner and contributed less to provisioning than N. vespilloides males. We can only speculate about the cause of this variation, but this uneven distribution may reflect differences in the strength of sexual conflict over parental investment in provisioning. To understand the striking variation in begging, provisioning and offspring dependency between species, we must also consider the different life-history strategies of burying beetles. For example, in a partial cross-fostering experiment, young of pied and collared flycatchers (Ficedula hypoleuca and Ficedula albicollis) have been shown to differ in their begging intensity (Qvarnström et al. 2007). The authors assumed that the difference in begging seems to honestly indicate intrinsic differences in the offspring that are likely linked to a differentiation in life-history traits. In the 3 species we examined, N. pustulatus is known to produce the largest number of offspring (Trumbo 1992; Capodeanu-Nägler et al. 2016). Thus, it may be necessary for offspring to maintain their independence as parents cannot attend to each larva as well as can parents of smaller broods (Trumbo 1992). Also, models predict that parental food provisioning only evolves if it is efficient relative to offspring self-feeding (Gardner and Smiseth 2011). In N. pustulatus, however, the large number of offspring (mean clutch size: 68 ± 19; see also Capodeanu-Nägler et al. 2016) hinders the efficient feeding of each larva in the brood, selecting against increased offspring dependency. In line with this, N. pustulatus parents provisioned significantly less than parents of the other 2 species. One other factor that could account for interspecific variation in begging, related to the nutritional dependence of offspring, is adult body size, as this is likely to influence growth rate and therefore offspring need. In burying beetles, larval weight at dispersal generally determines adult body size (Trumbo 1990) and we might expect that larger species are characterized by higher larval growth rate, which can only be accomplished by higher provisioning and begging efforts. Indeed, our results show that the 2 larger species, N. pustulatus and N. orbicollis, required less time for attaining their final body mass at dispersal than N. vespilloides, the smallest of the 3 species. However, this faster growth rate is not necessarily associated with a higher provisioning and begging rate, as begging intensity and levels of food provisioning were considerably lower in N. pustulatus than in N. vespilloides. Thus, when considering N. pustulatus, it seems rather unlikely that body size is the main determinant of how interactions between offspring and parents have evolved. Interestingly, although N. vespilloides larvae had overall the slowest growth rate, during the first 48 h, in which offspring begging and parental provisioning is most intense (Smiseth et al. 2003; Smiseth et al. 2007), they grew much faster than N. pustulatus larvae. Thus, while self-feeding in N. pustulatus appears to be sufficient to sustain the body functions of the hatchlings, parental provisioning in N. vespilloides seems to accelerate larval growth. Burying beetles represent an ideal model organism to explore the integration of offspring begging and parental provisioning once parental care has evolved because, within this genus, closely related species vary substantially in their reliance on parental food provisioning. Future studies might profitably employ cross-fostering among the 3 species to evaluate whether there is a positive correlation between offspring behavior of the recipient species and parental provisioning of the caregiving species. In combination with a consideration of various life-history strategies in this genus, this would help us to understand the emergence of the substantial differences in offspring dependence that have arisen within the genus. We recognize that the conclusions of our study are based on evidence derived from only 3 species, and are thus essentially qualitative with respect to between-species correlations. In a broader context, more comparative studies concerning offspring begging behavior and parental provisioning that also control for phylogeny are needed to further unravel the evolutionary trajectories and diversification of parental care. SUPPLEMENTARY MATERIAL Supplementary data are available at Behavioral Ecology online. FUNDING This work was supported by a grant from the German Research Foundation (DFG) to S.S. (grant number STE 1874/6-1) and a grant from the National Science Foundation (grant number IOS-1118160) to S.K.S. 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Published: Jan 1, 2018

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