Behavioral Ecology Advance Access originally published online on June 4, 2007
Behavioral Ecology 2007 18(4):730-735; doi:10.1093/beheco/arm038
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Extreme gender-based post-fledging brood division in the toc-toc
a Centre for Wildlife Assessment & Conservation, The University of Reading, Whiteknights PO Box 228, Reading RG6 6AJ, UK b Nature Seychelles, The Centre for Environment & Education, PO Box 1310, Roche Caiman, Mahe, Republic of Seychelles c Centre for Ecology, Evolution and Conservation, School of Biological Sciences, University of East Anglia, Norwich NR4 7TJ, UK
Address correspondence to D.S. Richardson. E-mail: david.richardson{at}uea.ac.uk.
Received 15 August 2006; revised 16 February 2007; accepted 1 April 2007.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The possibility that parents of one sex may preferentially invest in offspring of a certain sex raises profound evolutionary questions about the relative worth of sons and daughters to their mothers and fathers. Post-fledging brood division—in which each parent feeds a different subset of offspring—has been well documented in birds. However, a lack of empirical evidence that this may be based on offspring sex, combined with the theoretical difficulty of explaining such an interaction, has led researchers to consider a gender bias in post-fledging brood division highly unlikely. Here we show that in the toc-toc, Foudia sechellarum, post-fledging brood division is extreme and determined by sex; where brood composition allows, male parents exclusively provision male fledglings, whereas female parents provision female fledglings. This is the first study to provide unambiguous evidence, based on molecular sexing, that sex-biased post-fledging brood division can occur in birds. Male and female parents provisioned at the same rate and neither offspring nor parent survival appeared to be affected by the sex of the parent or offspring, respectively. The current hypotheses predicting advantages for brood division and preferential care for one specific type of offspring are discussed in the light of our results.
Key words: brood division, gender, offspring sex, parental care, provisioning behavior.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Socially monogamous mating systems with biparental care have evolved from promiscuous mating systems with no parental care, and the development of care-giving behavior has probably coevolved gradually with altriciality (Burley and Johnson 2002
). In some species, the high dependency of altricial offspring has led, through an evolutionary tendency toward more beneficial and cost effective parental investment, to parents preferentially directing care to subsets of offspring (reviewed in Lessells 2002). The specific functions and benefits of such parental bias are still unclear and more than one factor might be operating within, and between, species (Harper 1985; Lessells 2002; Wheelwright et al. 2003). One intriguing possibility, that raises profound evolutionary questions about the relative worth of sons and daughters to their mothers and fathers, is that parents of one sex may preferentially invest in offspring of a certain sex (Lessells 2002).
Post-fledgling brood division, a form of parental care allocation in birds, occurs when the care of specific subsets of offspring in a brood is divided between the parents (Smith 1978; McLaughlin and Montgomerie 1985; Slagsvold 1997; Leedman and Magrath 2003; Wheelwright et al. 2003). In some species, this division of care is expressed in some broods as a preference by a parent to invest in one particular offspring within the brood, but not at the total exclusion of the other offspring (Harper 1985; Byle 1990; Droge et al. 1991; Kopachena and Falls 1991). In other species, the care is exclusive but only for some members of the brood (Anthonisen et al. 1997; Leedman and Magrath 2003) or under certain circumstances, such as during the last brood of the season or specific (harsh) years (Edwards 1985; Price and Gibbs 1987; Vega Rivera et al. 2000). Extreme post-fledging brood division—when parents exclusively feed one subset of offspring—is not uncommon and has been documented across a range of species, such as song sparrows, Melospiza melodia (Smith 1978), northern wheatears, Oenanthe oenanthe (Moreno 1984), and Lapland longspurs, Calcaris lapponicus (McLaughlin and Montgomerie 1985).
It has long been hypothesized that brood division in birds could be selected to be based on offspring sex (Harper 1985; Lessells 2002). For instance, parents caring for fledglings of the same sex could avoid future inbreeding by reinforcing kin recognition (McLaughlin and Montgomerie 1985) and also reduce investment in the sex most likely to eventually compete for mates and territories (Harper 1985). However, there is, as yet, no clear evidence that this occurs. The only 2 studies that provide any quantitative evidence for this phenomenon—on the European robin, Erithacus rubecula (Harper 1985), and the dunnock, Prunella modularis (Byle 1990)—are undermined by extremely small sample sizes, incomplete sexing, and indirect methods of sexing (e.g., biometrics), which make it impossible to determine whether division was based on size or sex. In studies of brood division in which the sex of the offspring could be determined accurately, sons and daughters were divided randomly between parents (Price and Gibbs 1987; Odgen and Stutchbury 1997; Leedman and Magrath 2003; Wheelwright et al. 2003). Indeed, brood division based on the sex of offspring is now considered unlikely due to the predicted costs incurred under this strategy, such as the potential refusal to feed the "wrong" sex offspring if one parent was lost or just one sex was produced in a brood (Leedman and Magrath 2003; Wheelwright et al. 2003). As a result, the most commonly accepted hypotheses relating to brood division predict advantages without regard to fledgling sex, such as minimization of brood predation by physically separating the offspring, thus reducing the risk of losing the entire brood (i.e., Smith 1978; Harper 1985; McLaughlin and Montgomerie 1985; Anthonisen et al. 1997; Odgen and Stutchbury 1997).
In the endemic toc-toc (or Seychelles fody), Foudia sechellarum, females incubate clutches of one or, more often, 2 eggs but both parents attend the young in the nest (Crook 1961; Kraaijeveld and Komdeur 2003). Nestlings fledge after approximately 16 days; however, post-fledging care lasts for approximately 2 months if a subsequent brood is produced but up to 4 months if it is the only or last brood of the season (Vega 2005). Single fledglings are fed exclusively by the female, but the care of 2 fledged siblings is divided between the parents (Brooke 1985; Vega 2005). Here we show that in this species, post-fledging brood division is extreme and determined by sex; where brood composition allows, male parents exclusively provision male fledglings, whereas female parents provision female fledglings. This is, to our knowledge, the first study to provide unambiguous evidence, based on molecular sexing, that sex-biased post-fledging brood division can occur in birds.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Study site and population
The Seychelles toc-toc (a weaver finch from the Ploceidae family) is a forest dwelling weaverbird endemic to the Seychelles islands. This socially monogamous, sexually dimorphic, passerine species is currently listed as vulnerable under International Union for Conservation of Nature guidelines due to its restricted range (Crook 1961
; BirdLife International 2000). The present study was conducted on Cousin Island Nature Reserve between February and August 2002, November 2002 to October 2003, and May to August 2004. Cousin is a small (ca., 29 ha), low lying granitic island that contains the highest toc-toc density in the Seychelles (Vega 2005). Toc-tocs feed mainly on invertebrate prey collected from the underside of leaves and branches, but they also exploit any available source of seed, fruit, and nectar (Crook 1961; Vega 2005). On Cousin, the reproductive bond between male and female toc-tocs normally lasts over many consecutive years during which the pair maintains a small breeding territory year round (Vega 2005). During the breeding season, both males and females participate in nest building but only the female incubates the clutch of one or, more often, 2 eggs (Crook 1961; Kraaijeveld and Komdeur 2003; Vega 2005). Males are generally more aggressive and protective of nest and young (Vega 2005). No differences in the dispersal pattern of the 2 sexes have been detected on Cousin (Vega 2005).
Parent–offspring interactions
All the individuals we caught were individually ringed with a unique combination of 3 color rings and a South African metal ring, which allowed us to identify them in the field. Nestlings were ringed and weighed (g) at 7–10 days old. Young from inaccessible nests were caught as fledglings 2–4 weeks after fledging when they became mobile and possible to catch using mist nets. We followed each fledgling until it was observed being fed or until 30 min had elapsed, whichever happened first. We considered the fledgling to have reached independence when it was no longer observed being fed by an adult bird but instead foraged alone in at least 2 consecutive 30-min observation periods. To compare the provisioning rate of male and female parents, we randomly selected 3 pairs of birds, with 2 fledglings each, from the closely monitored families and observed them for 3 continuous hours during which all instances of feeding were recorded. Additionally, we opportunistically recorded the behavior of another 52 fledglings observed interacting with adult birds at least twice.
Molecular sexing
We collected blood samples (ca., 15 µl) from all nestlings and fledglings by brachial venipuncture and diluted them in 800 µl of 100% ethanol in a 2.0-ml screw-cap microfuge tube that was stored at room temperature. Blood samples were processed for DNA extraction as described in Richardson et al. (2001), and molecular sexing was undertaken using the polymerase chain reaction method devised by Griffiths et al. (1998).
Survival
During the first week of every month throughout the study period, we conducted a survey of the toc-toc population as follows: 1) 28 evenly distributed points on the island were visited on the same day of each month, and at each point, all toc-tocs observed within 2 min were recorded, 2) intense mist netting was undertaken for at least 3 days on the first week of each month in feeding/drinking areas known to be common to all the toc-tocs, and all birds caught were recorded, and 3) the breeding territory of each closely monitored family was visited at least twice during the first week of each month, and all toc-tocs sighted during 30 min were recorded. It is important to note that the toc-toc population on Cousin Island is isolated, and emigration to nearby islands, such as Cousine, is rare or nonexistent (Vega 2005).
Analysis
We analyzed offspring survival data using the program MARK (White and Burnham 1999). A simple 2-sex class model was produced to suitably demonstrate the effect of sex on the survival (
) and resighting probability (P) of offspring. Subsequently, a 2-sex class model was developed to investigate the effect of care-giving parent sex on the survival () and resighting probability (P) of offspring. The most parsimonious models were selected from a range of candidate models using the corrected Akaike's information criterion (AICc). The difference between the AICc in models should exceed 2 or be considered nearly tied and subsequent inference should be based on the subset of these models (Anderson and Burnham 1999). We used a goodness of fit bootstrap to assess the fit of models to the data with a hundred replicates run. The care-giving parent survival data were inadequate for analysis in program MARK. Adult birds were caring for fledglings at different times during the 2002 and 2003 season, and the adult survival rate was variable over time. Sample size was not powerful enough to allow us to perform separate analyses for different seasons and periods within the season. Therefore, inference on the care-giving parent survival was only obtained with a chi-square test.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Parent–offspring interactions
In the 2002 and 2003 breeding seasons, a total of 22 first brood nests from different breeding territories were closely monitored. Of these, 13 successfully fledged 2 young and 9 fledged just one. The 35 fledglings were closely monitored during the care-giving post-fledging period for an average of 12 weeks (range 8–16). On average, each fledgling was observed being fed 10.89 times (standard deviation = 3.36; range 6–18), with each observation separated by at least 5 days, providing a total of 479 independent feeding instances throughout the fledgling care period. Each fledgling monitored was consistently fed by the same single adult toc-toc throughout its period of post-fledging dependency. The statistical probability of this pattern being observed by chance was virtually zero (0.5479).
Of the 22 closely monitored nests, 11 broods fledged both a male and a female offspring. In every case, the female parent was observed to provide all the post-fledging care for the female offspring, whereas the male parent always cared for the male offspring (
2 = 22, degrees of freedom [df] = 2, P < 0.001; Table 1). In 2 broods, both containing 2 female offspring, each parent cared exclusively for one of the female offspring, whereas the 9 fledglings produced in single broods were always cared for entirely by the female parent irrespective of the sex of the fledgling (Table 1).
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An extra 243 feeding instances were recorded during prolonged observations on 3 sets of siblings (mean: 40.5 ± 15.51 feeding instances per fledgling observed for an average of 121.67 ± 48.34 min) interacting with their respective care-giving parent. There was no significant difference between the amount of feeds provided by the male parent in comparison with the female parent to specific fledglings of similar age (
2 = 1.74, df = 5, P = 0.88).
Out of the 52 additional fledglings that were opportunistically observed interacting with adult toc-tocs, male fledglings were significantly more likely to be associated with adult male toc-tocs, whereas female fledglings were significantly more likely to be associated with adult female toc-tocs (2 = 6.07, df = 1, P = 0.01; Table 2). The statistical significance of these post-fledgling association between the parent and offspring of the same sex was increased when the fledglings from the closely monitored nests were included in the analysis (2 = 21.83, df = 1, P < 0.001).
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Measurements were taken to determine the relative size of the nestlings to determine whether the brood division was based on size and not sex per se. Only 8 accessible nests contained more than one nestling (7 with different sexes and 1 with both female fledglings). On 4 occasions, the male parent eventually cared for the smallest chick (based on body mass) and in the other 4 cases, the male parent ended up caring for the largest chick.
Survival
It was assumed that the extra 52, opportunistically observed fledglings, were also cared for exclusively by the adult bird that was observed interacting with it, and the sample was combined with that from the closely monitored nests before performing the survival analysis. The 4 most parsimonious candidate models investigating the significance of sex and care-giving parent sex on the survival and resighting probability of offspring are presented in Table 3. Models I–IV consider the effect of offspring sex and Model I, which infers that the survival of the offspring was constant over time and not affected by the sex of the offspring, was 2.94 times better supported by the data than the next most parsimonious model (Model II). The resighting probability for the offspring was not affected by the sex of the offspring but was time dependent. Models V–VIII consider the effect of the care-giving parent sex, and Model V, which infers that the survival of the offspring was constant over time and not affected by the sex of the care-giving parent, was 3.67 times better supported by the data than the next most parsimonious model (Model VI). Again the resighting probability of the offspring was not affected by the sex of the care-giving parent, but it was time dependent. Finally, the probability of survival to the next breeding season for care-giving male and female parents was not significantly affected by the specific sex of the offspring cared for (2 = 0.003, df = 1, P = 0.954; 2 = 0.076, df = 1, P = 0.782, respectively; Table 4).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Our results show that post-fledging brood division among toc-tocs on Cousin Island was extreme and consistent over time. After leaving the nest, all provisioning to a single specific offspring was provided by the same parent throughout the fledgling care period. Furthermore, division of the brood was strongly associated with the sex of the parent and of the offspring. If fledglings of both sexes occurred within a brood, then the female parents exclusively cared for the female fledgling, whereas the male parent cared for the male offspring. Fledgling size did not appear to influence this pattern of extreme brood division.
The division of labor between feeding parents during the post-fledging care period has been attributed to, among other factors, the maximization of parental energy expenditure and to the better regulation of food partitioning between siblings (Wheelwright et al. 2003). Brood division would enable parents to concentrate on fewer offspring, consequently curtailing the search and travel times between offspring and also facilitating the regulation of food delivered to each offspring (Smith 1978; Moreno 1984). This explanation appears unlikely in the toc-tocs as, under this hypothesis, we would expect single fledglings to be cared for only by the male parent, thus enabling the female to perhaps start a new clutch. Furthermore, the simple regulation of food provided to a brood of 2 could have evolved in undivided broods if, for example, each parent alternately fed each fledgling.
Extreme brood division has been also hypothesized to be a strategy designed to maximize fledgling survival. The formation of 2 spatially divided family units may reduce the risk of the entire brood being preyed upon and also allow parents to ensure that less dominant fledglings receive a satisfactory share of food (McLaughlin and Montgomerie 1985). This hypothesis also seems unlikely to explain brood division in the toc-toc for a number of reasons. First, this species is a typical oceanic island bird that has evolved in an environment free from mammalian predators. Indeed, on Cousin Island, the risk of predation during the toc-toc post-fledging care period is extremely low, or nonexistent, as the only potential predators are 2 species of relatively small native skinks (Vega 2005). Second, the brood division observed in the toc-toc was not necessarily coupled with the spatial separation of siblings as would be predicted under this hypothesis. Toc-toc family units were commonly observed in the same area (within a couple of meters) throughout the post-fledgling care period. Consequently, brood division would not reduce the chance of the dominant fledgling monopolizing parental provisioning.
Another hypothesis has suggested that brood division might be driven by the dominant fledgling choosing, and monopolizing, the parent that is able to provision most (Slagsvold 1997; Leedman and Magrath 2003). However, in the toc-toc brood, division occurred immediately on fledging when the young had underdeveloped wing feathers and were mostly stationary receiving care from a single parent flying back and forth. At this point, without the ability to fly after the provisioning parent, it is hard to imagine that a fledgling could monopolize one of the parents. Further evidence against this hypothesis is provided by the data that show that the heaviest—and therefore presumably dominant—fledgling of a brood was equally likely to be fed by either parent. Furthermore, the amount of care provided by male and female parents during the postfledgling period was similar, as was the subsequent survival probability of fledglings cared for by either parent.
Recently, the general hypothesis based on reduced predation risk and/or improved feeding efficiency has been considered incomplete (Vega Rivera et al. 2000) or inadequate to predict long-term brood division (Leedman and Magrath 2003). Factors, other than brood survival and management, have been put forward as important in the parent's decision to divide the brood. For instance, not dividing the brood may facilitate the males' ability to mate guard the female before the next clutch of the season (Vega Rivera et al. 2000). Furthermore, it has been emphasized that the predation and feeding efficiency hypotheses do not necessarily predict the exclusive care of specific offspring by individual parents but only the division of the brood (Leedman and Magrath 2003). A new hypothesis based on the development of a social specialization between the parent and the offspring does, however, predict extreme and long-term brood division. This division would benefit both the feeding parent and the young as they progressively become better at mutual interactions based on alarm and feeding call recognition and on learnt features, such as fledgling's hiding places and fledgling's flight ability (Leedman and Magrath 2003). However, the benefits incurred during such a prolonged interaction may not necessarily be the function selecting for brood division but only for the extreme and stable separation of subsets of offspring in an already divided brood. For instance, in the toc-toc, the benefits of the social specialization hypothesis could be achieved in undivided broods by having both parents and fledglings interacting together for a prolonged and continuous period.
Preemptive desertion of a subset of the brood by the parent that provides more care has been suggested to explain brood division (Lessells 2002). This is based on the assumption that the parent that provisions less benefits from undivided broods, whereas the parent that provisions more benefits under divided broods. This hypothesis has been supported by recent theoretical modeling as a primary function of the evolution of brood division among biparental species (Lessells 2002). In the toc-toc, females provision significantly more often than do males during the nestling period that lasts 13–15 days (Vega 2005). Males would theoretically, therefore, benefit from an undivided brood during the postfledging period, which can extend up to 4 months (Vega 2005), as the females would compensate for their lower feeding rates. This line of reasoning suggests that it is the female parent that instigates brood division in the toc-toc. By exclusively feeding only a single fledgling, the female may be forcing the male to contribute equally during the extended period of parental investment. The preemptive desertion strategy would also result in only one parent caring for fledglings in broods of one, even when both parents are potentially available to care (Leedman and Magrath 2003). This all-or-no-care rule of thumb appears to be supported in the toc-toc; first, male toc-tocs did not feed begging single fledglings even when they were nearby and second, in families that eventually lost one of the 2 fledglings, the remaining fledgling was ignored by the extra available parent, even if it was the female parent and even when it was nearby (Vega L, personal observation). It is also possible that extrapair paternity could also be influencing patterns of brood division and parental investment in this population. For example, lower confidence of paternity compared with maternity may explain why the care of single offspring is by the female only. Unfortunately, we have no information on extrapair paternity for this species. Importantly, neither the hypothesis of preemptive desertion described here nor any of the other hypotheses outlined above explain on their own why brood division should be sex biased.
Theoretical models predict that biased parental care is favored by selection and should be more intense and widespread than actually observed in most bird species and, if the bias is toward a specific type of offspring (sex), then it should evolve to an extreme (Lessells 2002). The post-fledging brood division by sex observed in the toc-toc supports the predictions of such models. However, the mechanisms and advantages of such strategy are not clear. The hypothesized advantages of sex-biased brood division have normally been based on an association occurring between a parent and fledgling of the opposite sexes (Harper 1985; McLaughlin and Montgomerie 1985; Wheelwright et al. 2003). Such an association would allow for kin recognition to be reinforced and for the avoidance of future inbreeding (McLaughlin and Montgomerie 1985). Importantly, it would also avoid investment in the sex most likely to eventually compete for mates and territories (Harper 1985). Nonetheless, the association found in the toc-toc is between parents and offspring of the same sex. Female toc-tocs only care for male offspring if there is no surviving female fledgling in the brood. Another hypothesis suggests that a specific type (sex) of adult may be better at caring for a specific type (sex) of offspring and that brood division optimizes the survival of the fledglings (Leedman and Magrath 2003). However, there is no evidence to suggest that this is the case in the toc-toc, as the survival of male and female fledglings did not appear to differ based on the sex of the care-giving parent. Furthermore, parental survival was not affected by the sex of the fledgling cared for. The same lack of a relationship between the sex of a care-giving parent and offspring survival was also found in Savannah sparrows (Wheelwright et al. 2003).
One possibility to explain the female toc-toc parents' bias toward female offspring could be related to sex-specific behavior. For instance, sex-specific foraging, singing, dispersal, and courtship behavior could either be learnt better from parents of same sex or, in the case of the foraging, might facilitate the parental care of the offspring (McLaughin and Montgomerie 1985). Even though neither adult nor juvenile toc-tocs on Cousin show distinctive difference in foraging strategy or dispersal ability between the sexes (Vega 2005), male and female toc-tocs do have distinctive territorial calls (Vega L, personal observation), and the courtship display observed among toc-tocs is sex specific (Crook 1961). Therefore, this hypothesis remains a possibility, but further research is necessary to test it.
Another possible explanation for the observed extreme sex-biased brood division is based on the hypothesis that the sex-based division of fledglings is purely a rule of thumb to maintain and facilitate the division of labor (Harper 1985). This raises the question of why sex is the best characteristic on which to base this divide and, importantly, how sex is identified. Birds are known to be able to discriminate between individuals and discern kin from non-kin using a range of cues (Komdeur and Hatchwell 1999), and adult birds can, quite obviously, recognize the sex of other adults even in sexually monomorphic species. It is therefore possible that adult birds can recognize the sex of their offspring perhaps, for example, through differences in sound, wing flapping, motion, and posture during begging interactions with parents (Lessells 1998). Further work is now required to investigate such possibilities and to understand the mechanisms responsible for sex recognition in the toc-toc.
In conclusion, our study shows that, in the Cousin Island population of toc-tocs, brood division is extreme and sex biased. This is the first time that sex-biased parental care of fledglings has been demonstrated unambiguously and contrasts with other recent studies that have suggested that such sex-biased provisioning is unlikely in birds (Leedman and Magrath 2003; Wheelwright et al. 2003). The evidence from this study does not support the idea that increased fledgling survival, feeding efficiency, and fledgling choice can be the evolutionary cause of this brood division. However, this study is merely correlative, and experiments are now required to test these possibilities more rigorously.
A hypothesis, in which a conflict of interest between parents in how parental care is divided is resolved by the splitting of the brood based on sex, was supported. In this scenario, female toc-tocs may actively select for a division of labor by dividing the brood and preemptively forcing the male to invest equally in fledgling care. In addition, the concept that sex-specific behaviors occur that might benefit the parental care of the same sex of offspring remains a possibility. Though whether such benefits are selected for or were merely an added advantage of sex-based brood division would be difficult to determine. Investigation of the mechanisms favoring and maintaining brood division in the toc-toc now requires the use of carefully thought out and controlled experiments (e.g., Kopachena and Falls 1991). Overall, the evidence presented here on extreme brood division with sex-biased parental care highlights a new predicament for brood division and its rich array of hypotheses.
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ACKNOWLEDGEMENTS |
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This study was funded by the University of Reading, the Royal Society for the Protection of Birds, and Nature Seychelles. The authors are thankful to Steve Parr, Nirmal Shah, Rachel Bristol, Joel Souyave, Ian Valmont, Dr David Currie, Janske Van de Crommenacker, Arjan Dekker, Cas Eikenaar, Lyanne Brouwer, Julia Everard, and Dr Malcolm Nicoll. D. S. Richardson was funded by a Natural Environment Research Council postdoctoral fellowship (NER/I/S/2002/00712).
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