Prenatal environmental conditions underlie alternative reproductive tactics that drive the formation of a mixed-kin cooperative society

  1. Shailee S. Shah
  2. Dustin R. Rubenstein

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    Evaluation Summary:

    This article will be of interest to evolutionary biologists and behavioural ecologists. It aims to quantify the fitness benefits of helping with the breeding attempts of others vs. seeking own breeding attempts via dispersal. It is generally considered that helping is less profitable than breeding, but occurs when superior reproductive options are constrained. Using a long-term dataset of birds, the authors call into question this assumption, and propose that both reproductive tactics can in fact have similar fitness returns, resulting in mixed-kin societies.

    (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 #1 and Reviewer #3 agreed to share their names with the authors.)

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Abstract

Although animal societies often evolve due to limited natal dispersal that results in kin clustering and facilitates cooperation among relatives, many species form cooperative groups with low kin structure. These groups often comprise residents and immigrants of the same sex that compete for breeding opportunities. To understand how these mixed-kin societies form, we investigated the causes and fitness consequences of dispersal decisions in male cooperatively breeding superb starlings ( Lamprotornis superbus ) inhabiting a climatically unpredictable environment. We show that the two alternative reproductive tactics—natal dispersal or philopatry—exhibit reproductive trade-offs resulting in equivalent lifetime inclusive fitness. Unexpectedly, an individual’s tactic is related to the prenatal environment its parents experience before laying rather than the environment it experiences as a juvenile. Individuals that adopt the tactic not predicted by prenatal environmental conditions have lower fitness. Ultimately, climate-driven oscillating selection appears to stabilize mixed-kin societies despite the potential for social conflict.

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  1. eLife

    Evaluation Summary:

    This article will be of interest to evolutionary biologists and behavioural ecologists. It aims to quantify the fitness benefits of helping with the breeding attempts of others vs. seeking own breeding attempts via dispersal. It is generally considered that helping is less profitable than breeding, but occurs when superior reproductive options are constrained. Using a long-term dataset of birds, the authors call into question this assumption, and propose that both reproductive tactics can in fact have similar fitness returns, resulting in mixed-kin societies.

    (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 #1 and Reviewer #3 agreed to share their names with the authors.)

  2. eLife

    Reviewer #1 (Public Review):

    This study uses a long-term dataset of cooperatively breeding starlings to calculate lifetime fitness of two different male strategies: natal philopatry (staying to help at the natal nest site) or dispersal. Both strategies co-occur in the study population, resulting in a "mixed-kin society". The authors test (1) whether pre-natal or post-natal environmental conditions can explain the likelihood of male dispersal, and (ii) whether dispersing results in higher lifetime fitness than staying at home.

    The results reveal that pre-natal environmental conditions, rather than post-natal conditions, are the best predictor of male dispersal (males disperse more when pre-natal conditions are good). The results also show that males that disperse have similar lifetime reproductive fitness to those that do not. The authors conclude that high variability in environmental conditions, such as occurs in the habitat of the study species, may generate mixed-kin societies, as such environments oscillate between favouring dispersal and favouring philopatry. The conclusions of the study are well-supported by the data.

    The authors discuss that the mechanisms explaining why pre-natal (and not post-natal) environmental conditions predict male dispersal are not known. They propose that parental effects (e.g. physiological or epigenetic) on offspring could explain this relationship. A possible alternative explanation that is not discussed is that parents' behaviour toward male offspring is affected by pre-natal conditions, such that parents sometimes force/encourage their sons' dispersal. In either case, the mechanisms underlying this observed relationship remain for future study.

    Overall, this study makes a valuable contribution to our understanding of the factors that drive vertebrates to either stay and help at the nest or disperse to new territory, and thus the drivers of mixed-kin societies containing both philopatric and dispersing individuals.

  3. eLife

    Reviewer #2 (Public Review):

    This paper attempts to go to heart of solving the evolutionary enigma of cooperative breeding - how can reproductive and non-reproductive helping strategies be maintained in a population? The typical suggestion is that helping is maintained by the indirect benefits of helping kin when more profitable breeding opportunities are constrained. Under this hypothesis, helping is the best of a bad job strategy. In this paper, the aim is to set this long-standing assumption against another possibility - that the two strategies offer comparable fitness, and so are maintained in the population as a type of polymorphism. However, testing whether offspring that remain philopatric accrue comparable or differential fitness from those that disperse to fight for breeding positions is challenging, and hence rare.

    There are a number of reasons for this. First, the best way of testing the fitness of different strategies in cooperative breeders is to do so in individuals living in the same group, since only then can effects of group size and territory quality be controlled. Second, one of the greatest difficulties however, is that those that remain resident and help versus disperse and breed have different genetics, rearing environments and qualities, meaning that any differences in fitness might be due to these differences rather than the strategies pursued. Finally, it is almost impossible to know what immigrants did before they arrived and what emigrants did after they left, meaning there is a missing fraction of fitness in the lives of most individuals.

    This study on superb starlings was able to overcome some of these issues, but not all. For example, residents and immigrants live and breed in the same groups, which allows one to compare fitness in the same groups and territories. However, whether individuals gained fitness after dispersing or before emigrating is not clear for most individuals, which will either lead to a missing fraction of fitness in individuals or a severely restricted sample with complete, but possibly biased, information. As a consequence, whether or not helping and breeding strategies offer equal fitness, as suggested, will likely require further study, but this present study paves the way for how one might begin to address these outstanding and central questions in cooperative breeding research, with implications for understanding cooperation in human societies.

  4. eLife

    Reviewer #3 (Public Review):

    This manuscript aims at better understanding why social groups with mixed or low kin structure occur in some cooperative species. The authors investigate the hypothesis that two alternative strategies of males (stay or disperse) can persist within a population if conditions fluctuate from year-to-year and the relative fitness payoffs of these strategies are environment-dependent. To do so, they use a highly commendable long-term dataset on superb starlings and investigate 1) the relationship between pre- or postnatal environment (group size, sex ratio and rainfall) and the likelihood to disappear from the study population around 1 year of age (assumed to be a dispersal event) 2) whether these presumed dispersal events occur more among individuals that have been seen alloparenting (suggesting that promoting alloparenting may be a way parents incentivize their offspring to stay in their natal group), 3) whether immigrants and residents differ in terms of various fitness measures and 4) whether differences in fitness may be environment dependent. The results suggest that 1) prenatal rainfall is linked to dispersal decisions, 2) alloparents are more likely to stay in their natal groups, 3) immigrants/dispersers and residents have similar fitness and 4) their fitness is condition dependent (fitness of one strategy is higher when prenatal conditions match the condition that favour this strategy). Therefore, this set of results are all in agreement with the initial hypothesis.

    The manuscript addresses an important and interesting question, represents an important amount of work (both fieldwork and analysis), is very well written, transparent, easy to follow with well-designed and informative figures. However, as it stands the robustness of some results seem weak due to three major potential issues:

    1. One cannot tell whether individuals categorised as "dispersed" did disperse or died. The authors do acknowledge this possibility in the Methods section but state that their result (more likely to disperse after high prenatal rain) is unlikely to be driven by mortality since the opposite relationship would then be expected. However, this is not necessarily true. For example, it has been suggested that females may decrease egg mass in poor environmental conditions if there is a greater positive effect of egg size on offspring survival under adverse conditions, and such patterns have been shown by several experimental studies.

    2. Similarly, it is unclear whether individuals categorized as "not alloparenting" were seen but not alloparenting, or were simply not seen (potentially dead). It seems to be the latter, which could easily lead to a spurious relationship between probability to be not seen alloparenting/die and probability to disperse/die. This is particularly problematic since it was apparently particularly common for individuals to be missed for multiple breeding seasons before being seen again, especially if they did not act as alloparents.

    3. Several potentially important random effects (season, cohort, or group identity effects) were omitted from most analyses. I understand that this was likely due either to issues with model convergence, and/or to odd error distributions (e.g. lifetime reproductive success, Tuljapurkar et al. 2020) pushing to use non-parametric tests. Nevertheless, ignoring these effects are likely to artificially increase the power of the analyses and therefore likely lead to overconfidence of the estimated effects.

    In addition to these methodological issues, there are a couple of potential misinterpretations of the results:

    1. The authors found no evidence for differences in lifetime inclusive fitness between Immigrants and Residents, suggesting that dispersers and residents have similar fitness. However, immigrants already dispersed and a cost of dispersal is highly expected. If such costs do exist, as suggested by the authors, then the dispersing strategy may have lower fitness benefits than the philopatric strategy. This needs to be acknowledged.

    2. It is suggested that females breeding after low rain indirectly promote philopatry by promoting alloparenting (because of the relationship between these two measures). The authors do have data to investigate this (keeping in mind the above-mentioned potential biases). However, the data do not seem to support this statement (replacing "dispersal/non dispersal" status by the "alloparent/non alloparent" status in the analyses lead to non-significant effects of prenatal rainfall).

  5. Version published to 10.1126/sciadv.abk2220
  6. Version published to 10.1101/2021.02.10.430612v2 on bioRxiv
  7. Version published to 10.1101/2021.02.10.430612v1 on bioRxiv