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Therefore, a high enough but variable level of resources throughout the year favors the evolution of persistent kin groups and cooperation outside the reproductive context, while an additional increase in the variation in productivity may act as the condition favoring the subsequent evolution of cooperative breeding. A recent comparative study suggested that high annual survival facilitates the evolution of cooperative breeding in birds [35].

High annual survival allows prolonged parental investment into offspring [16,47] by providing offspring an incentive to remain with the parents beyond independence [38].

Moreover, it favors a delayed onset of independent reproduction [26], making cooperative breeding adaptive, particularly in variable environments where helpers at the nest can buffer reproductive failure in harsh years [6]. Our findings provide novel insights into the geographic distribution of different social systems, which has currently defied full explanation [9].

We speculate that the answer lies with an increase in the within year variance in environmental productivity. For example, several of the previously identified geographic hotspots of cooperative breeding Southern Africa, Australia, Northern South America; [9] underwent drastic climatic changes throughout the Eocene, from subtropical and tropical climates to seasonal savanna habitats or arid environments [54].

Accordingly, these environmental changes suggest these hotspot locations likely changed over time from favoring family living to favoring cooperative breeding.

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In conclusion, our analyses reveal 2 key findings that provide a novel way of understanding the evolution of cooperation in birds and suggest a resolution for earlier equivocal findings [6,7,9,10,23]. First, family living enables coping with variable environmental conditions and increases offspring survival both within and outside the breeding season [38].

Subsequently, it sets the scene for the secondary evolution of cooperative breeding [5] when environments have become more variable throughout the year and during the breeding season. Second, we found that cooperative breeding among unrelated individuals is exceptional and likely has different evolutionary origins than family-based cooperative breeding S2 Fig. Previous work suggested that this form of cooperative breeding arose through an alternative pathway, namely direct fitness benefits from reproductive sharing [13].

Overall, our analysis shows that considering path dependence is essential for understanding the evolution of complex adaptations, such as cooperative breeding, that may involve multiple independent evolutionary steps to be achieved [55]. We used 3 different criteria to differentiate between the different social systems, using the known duration of family associations i. We did not categorize occasional cooperative breeding species as cooperative breeders [1] based on the first 2 criteria above.

Occasional cooperative breeding resembles interspecific feeding, in which individuals feed offspring of another species, and thus, different factors are likely to be associated with occasional cooperative breeding and regular cooperative breeding [1]. Species were categorized as sedentary maximally engage in local movements or migratory short-, long-distance, and altitudinal migrants.

Nest type was categorized as a binary variable cavity breeders: nests in cavities, cliffs, and caves; other nests: all other nest constructions. We used the mean body weight combining male and female weight and distinguished precocial from altricial species categorizing semiprecocial species as precocial and semialtricial species as altricial. We calculated for each species:. Since the variance often increases with the mean i. Thus, we re-ran our analyses using the coefficient of variance where appropriate for variables measured on absolute scales, i.

Both the PCA S4 Table and the multinomial model S5 Table resulted in qualitatively similar results as our main analyses, indicating that our choice of variability metric did not bias our results. Ancestral state estimation was performed using the MuSSE function of the Diversitree package [28] on a consensus phylogeny estimated from a sample of 1, phylogenetic trees [27] with the maximum parsimony matrix method using the Hackett tree backbone.

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We note that using a consensus phylogeny with the Ericsson backbone returned qualitatively identical results. Also, using a model in which speciation and extinction rates were allowed to vary resulted qualitatively in the same results as the main models with diversification rates fixed to be equal across breeding modes S6 Table. We fitted phylogenetically controlled multinomial models to our data using MCMCglmm [29]. The response variable in all models was a categorical representation of social system 3 nominal levels: non-family living, family living, and cooperative breeding.

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The phylogenetic random effect was modelled based on a recent phyla-wide phylogeny [27]. To account for the uncertainty of phylogeny estimation, we refitted the main model with 50 randomly selected trees from the posterior distribution of trees published in Jetz et al. Given that ancestral character reconstruction may be biased when characters influence diversification [60], we also used a phylogenetic controlled PCA phyloPCA function in phytools [59], resulting is a somewhat different PC structure S7 Table.

However, running our main model with this PC resulted qualitatively in the same results S8 Table. You must be logged in to post a comment. Biology Environmental Sciences. Caerlos Botero. No Comments.

Introduction Cooperative breeding is an extreme form of cooperation that occurs when individuals help raise conspecific offspring that are not their own [1], often while temporarily foregoing their own reproduction [2,3]. Fig 1. Avian social systems. Results Given the rarity of non-kin helping see above , we began our analyses by focusing on the 3 major avian social systems i. Discussion Overall, our results help unravel the potential sequence of evolutionary steps in the evolution of cooperative breeding and provide a clearer picture of the role of ecoclimatic factors in this process.

We calculated for each species: Precipitation: mean, within and between year variance, predictability during the whole year; Precipitation: mean, within and between year variance during the MGS only; Temperature: mean, within and between year variance, predictability during the whole year; Temperature: mean, within and between year variance during the MGS only; NPP: mean, variance, predictability during the whole year; NPP: mean, within and between year variance, predictability during the MGS only; MGS length; Habitat heterogeneity according to [57]. Occasional cooperative breeding in birds and the robustness of comparative analyses concerning the evolution of cooperative breeding.

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Evolutionary routes to non-kin cooperative breeding in birds. Family living: an overlooked but pivotal social system to understand the evolution of cooperative breeding. Behavioral Ecology. Prevalence of different modes of parental care in birds. Theoretical Population Biology. Avian life histories: Is extended parental care the southern secret? Life history and the evolution of family living in birds.

Promiscuity and the evolutionary transition to complex societies. Life histories and the evolution of cooperative breeding in mammals. Ancestral monogamy shows kin selection is key to the evolution of eusociality. Cooperation facilitates the colonization of harsh environments. Speciation in the wrens of the genus Campylorhynchus. University of California Publications in Zoology. Population ecology of the cooperative breeding acorn woodpecker. Princeton: Princeton University Press; Lifespan and reproductive costs explain interspecific variation in the optimal onset of reproduction.

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Introduction

Vilela B, Villalobos F. Sex, long life and the evolutionary transition to cooperative breeding in birds. Proc R Soc B. Global gradients of avian longevity support the classic evolutionary theory of ageing. Cooperative breeding in birds: the role of ecology.