Experimental evidence that group size generates divergent benefits of cooperative breeding for male and female ostriches
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Evaluation Summary:
This manuscript is of broad interest to readers in the field of animal behavior and the evolution of cooperation. This work experimentally investigates the effect of differences in group size and group composition on reproductive behavior, by using an impressive sample of semi-wild populations of ostriches. While the paper does not address some aspects of groups, such as relatedness and parentage, overall, this paper is a complete analysis of the breeding ecology of this system and can serve as a blueprint for more of such work in the fields of cooperation, group living and breeding ecology.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #2 agreed to share their name with the authors.)
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Abstract
Cooperative breeding allows the costs of parental care to be shared, but as groups become larger, such benefits often decline as competition increases and group cohesion breaks down. The counteracting forces of cooperation and competition are predicted to select for an optimal group size, but variation in groups is ubiquitous across cooperative breeding animals. Here, we experimentally test if group sizes vary because of sex differences in the costs and benefits of cooperative breeding in captive ostriches, Struthio camelus, and compare this to the distribution of group sizes in the wild. We established 96 groups with different numbers of males (1 or 3) and females (1, 3, 4, or 6) and manipulated opportunities for cooperation over incubation. There was a clear optimal group size for males (one male with four or more females) that was explained by high costs of competition and negligible benefits of cooperation. Conversely, female reproductive success was maximised across a range of group sizes due to the benefits of cooperation with male and female group members. Reproductive success in intermediate sized groups was low for both males and females due to sexual conflict over the timing of mating and incubation. Our experiments show that sex differences in cooperation and competition can explain group size variation in cooperative breeders.
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Evaluation Summary:
This manuscript is of broad interest to readers in the field of animal behavior and the evolution of cooperation. This work experimentally investigates the effect of differences in group size and group composition on reproductive behavior, by using an impressive sample of semi-wild populations of ostriches. While the paper does not address some aspects of groups, such as relatedness and parentage, overall, this paper is a complete analysis of the breeding ecology of this system and can serve as a blueprint for more of such work in the fields of cooperation, group living and breeding ecology.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #2 agreed to share their name with the …
Evaluation Summary:
This manuscript is of broad interest to readers in the field of animal behavior and the evolution of cooperation. This work experimentally investigates the effect of differences in group size and group composition on reproductive behavior, by using an impressive sample of semi-wild populations of ostriches. While the paper does not address some aspects of groups, such as relatedness and parentage, overall, this paper is a complete analysis of the breeding ecology of this system and can serve as a blueprint for more of such work in the fields of cooperation, group living and breeding ecology.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #2 agreed to share their name with the authors.)
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Reviewer #1 (Public Review):
In general, I consider that the manuscript reflects a huge effort in terms work done and data collection, the manuscript is very well written, and it brings new knowledge in terms of cooperative breeding and its connection with groups size in ostrich. My major concerns are about the title and introduction that are in my opinion too broad and not enough detailed.
In the introduction the scientific background that led to this research is lacking, and the manuscript would benefit from a more supported introduction, which makes it difficult to understand how far this study went comparatively to previous studies.
The research work was well conducted, and adjusted to the study aims. However, it would benefit from including more details on the observational data collected by the authors.I think the research topic …
Reviewer #1 (Public Review):
In general, I consider that the manuscript reflects a huge effort in terms work done and data collection, the manuscript is very well written, and it brings new knowledge in terms of cooperative breeding and its connection with groups size in ostrich. My major concerns are about the title and introduction that are in my opinion too broad and not enough detailed.
In the introduction the scientific background that led to this research is lacking, and the manuscript would benefit from a more supported introduction, which makes it difficult to understand how far this study went comparatively to previous studies.
The research work was well conducted, and adjusted to the study aims. However, it would benefit from including more details on the observational data collected by the authors.I think the research topic is interesting, and the study was well performed, but the manuscript would benefit from a more clear approach to the working hypothesis, expected results and background theories/hypotheses.
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Reviewer #2 (Public Review):
This work sets out to investigate experimentally the effect of differences in group size and group composition on reproductive behavior and success in ostrich groups. Direct field observations of the relationship between group composition/group size and reproductive success, do not allow for causal inference, as there may be several reasons why patterns may arise. For example, observing individuals having a higher reproductive success in larger groups than in smaller groups may not be a direct result of a larger group size per se, but it may be that higher quality individuals manage to establish themselves more often in larger groups. Hence, experimental manipulation of group size and group condition in natural contexts is important. 96 experimental groups of ostriches were established in fenced off areas in …
Reviewer #2 (Public Review):
This work sets out to investigate experimentally the effect of differences in group size and group composition on reproductive behavior and success in ostrich groups. Direct field observations of the relationship between group composition/group size and reproductive success, do not allow for causal inference, as there may be several reasons why patterns may arise. For example, observing individuals having a higher reproductive success in larger groups than in smaller groups may not be a direct result of a larger group size per se, but it may be that higher quality individuals manage to establish themselves more often in larger groups. Hence, experimental manipulation of group size and group condition in natural contexts is important. 96 experimental groups of ostriches were established in fenced off areas in the Karoo in South Africa, varying the number of males (1 / 3) and the number of females (1 / 3 / 4 / 6) across groups. Groups were followed for almost a year, studying a period without parental care (eggs were removed and incubated in an incubator to measure reproductive success) and a period with parental care (eggs were left in the enclosures). In the latter case, behavioral observations were done to study nest incubation, and sexual conflict (interruptions of incubation). The study was done for seven years, and having such data on experimental manipulations in semi-wild conditions is very valuable. The combination of behavioral analysis, with careful tracking of the fate of eggs (by daily nest checks), the experimental nature, and measuring reproductive success make for a very complete analysis of the breeding ecology of this system and can serve as a blueprint for more of such work in the fields of cooperation, group living and breeding ecology.
Some aspects, however, deserve more attention. First, at present, the origin and familiarity and possible relatedness among the group members of the experimentally composed groups is not discussed, and it may be that these factors play a role in shaping the results. Second, the reproductive measure used was the average number of chicks per sex, but it was not calculated at the individual level. There were no genetic analysis done to establish which individuals were actually successful in terms of reproduction. Since individual level selection is likely very important in this system, the results of average reproductive success need to be interpreted with great care. Third, the study was done under semi-natural conditions, meaning that the effects of other factors possibly shaping the success of group size and group composition in the wild (e.g., possible nest predation) were weakened. Finally, a closer connection between the experimental results on optimal group size, and whether this can actually be found in the dataset on natural variation in group size and group composition can be explored.
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Author Response
Reviewer 1
In general, I consider that the manuscript reflects a huge effort in terms work done and data collection, the manuscript is very well written, and it brings new knowledge in terms of cooperative breeding and its connection with groups size in ostrich. My major concerns are about the title and introduction that are in my opinion too broad and not enough detailed.
In the introduction the scientific background that led to this research is lacking, and the manuscript would benefit from a more supported introduction, which makes it difficult to understand how far this study went comparatively to previous studies. The research work was well conducted, and adjusted to the study aims. However, it would benefit from including more details on the observational data collected by the authors.
I think the research …
Author Response
Reviewer 1
In general, I consider that the manuscript reflects a huge effort in terms work done and data collection, the manuscript is very well written, and it brings new knowledge in terms of cooperative breeding and its connection with groups size in ostrich. My major concerns are about the title and introduction that are in my opinion too broad and not enough detailed.
In the introduction the scientific background that led to this research is lacking, and the manuscript would benefit from a more supported introduction, which makes it difficult to understand how far this study went comparatively to previous studies. The research work was well conducted, and adjusted to the study aims. However, it would benefit from including more details on the observational data collected by the authors.
I think the research topic is interesting, and the study was well performed, but the manuscript would benefit from a more clear approach to the working hypothesis, expected results and background theories/hypotheses.
We are very grateful for the positive and constructive feedback. The title and introduction have been revised according to the reviewer’s suggestions. We provide a more extensive introduction to the hypotheses being tested, which are now explicitly stated. The observational data we collected have been described in more detail and we integrate our observational and experimental data more thoroughly.
In the evaluation summary, the reviewer highlights that we did not address some aspects of groups, such as relatedness and parentage. We have now added additional analyses to show these do not change the conclusions of our study (for details please see responses to reviewer 2 who raises similar concerns more extensively). These were not originally included in the manuscript as the aim of our study was to examine how group size and composition influence the average reproductive success for any given individual, irrespective of variation in relatedness and parentage within groups.
Reviewer 2
This work sets out to investigate experimentally the effect of differences in group size and group composition on reproductive behavior and success in ostrich groups. Direct field observations of the relationship between group composition/group size and reproductive success, do not allow for causal inference, as there may be several reasons why patterns may arise. For example, observing individuals having a higher reproductive success in larger groups than in smaller groups may not be a direct result of a larger group size per se, but it may be that higher quality individuals manage to establish themselves more often in larger groups. Hence, experimental manipulation of group size and group condition in natural contexts is important. 96 experimental groups of ostriches were established in fenced off areas in the Karoo in South Africa, varying the number of males (1 / 3) and the number of females (1 / 3 / 4 / 6) across groups. Groups were followed for almost a year, studying a period without parental care (eggs were removed and incubated in an incubator to measure reproductive success) and a period with parental care (eggs were left in the enclosures).
In the latter case, behavioral observations were done to study nest incubation, and sexual conflict (interruptions of incubation). The study was done for seven years, and having such data on experimental manipulations in semi-wild conditions is very valuable. The combination of behavioral analysis, with careful tracking of the fate of eggs (by daily nest checks), the experimental nature, and measuring reproductive success make for a very complete analysis of the breeding ecology of this system and can serve as a blueprint for more of such work in the fields of cooperation, group living and breeding ecology.
Some aspects, however, deserve more attention. First, at present, the origin and familiarity and possible relatedness among the group members of the experimentally composed groups is not discussed, and it may be that these factors play a role in shaping the results. Second, the reproductive measure used was the average number of chicks per sex, but it was not calculated at the individual level. There were no genetic analysis done to establish which individuals were actually successful in terms of reproduction. Since individual level selection is likely very important in this system, the results of average reproductive success need to be interpreted with great care. Third, the study was done under semi-natural conditions, meaning that the effects of other factors possibly shaping the success of group size and group composition in the wild (e.g., possible nest predation) were weakened. Finally, a closer connection between the experimental results on optimal group size, and whether this can actually be found in the dataset on natural variation in group size and group composition can be explored.
We are very grateful for the careful review of our work and positive feedback. The suggestions and comments have been extremely helpful in revising the manuscript, which have led to the following changes:
We have added details about the origin and familiarity of group members, together with extra analyses verifying that our results are not confounded by variation in within-group relatedness. The study population has a nine-generation pedigree allowing us to accurately estimate relatedness between individuals. In the design phase of the experiment, relatedness amongst individuals was kept low in accordance with data from natural populations, but there were related individuals of the same sex in some groups. We tested if the average relatedness within groups influenced the average number of chicks individuals produced and found no significant relationship (Supplementary file 1 – Tables S16 and S17).
We have included genotyping analyses of 3227 offspring to verify that our non-genetic estimates of average reproductive success per sex (total chicks produced by groups / number of same sex individuals) accurately reflect measures obtained using genetic estimates of individual reproductive success. Genetic and non-genetic measures were highly correlated (R >0.95). We have added these verification analyses to the manuscript. The text has also been edited to further clarify that our aim is to estimate the average reproductive benefits for any given individual of being in group of a particular size, rather than examining differences in reproductive success between individuals within groups, for which genetic methods are required.
We have clarified the advantages and limitations of experimental studies. As reviewer 2 highlights, observational studies alone do not provide causal insight into the factors influencing group size, but as reviewer 1 indicates, experimental studies can lack ecological context. Consequently, both have their merits. Experimental manipulations of entire social groups are currently lacking on large vertebrate cooperative breeders, but can be used to estimate the costs and benefits of living in different group sizes that arise independently of ecological conditions. The results of such experimental studies can be used as a benchmark against which other data can be compared, such as observational data on wild groups subject to ecological pressures, including nest predation. The discrepancies between experimental and observational data can then be used to infer the relative importance of social versus ecological factors in shaping social groups.
We have added a figure (Figure 1 - figure supplement 1) and extended the discussion to better connect our experimental data with our observations of natural variation in group size.
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